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Soil beneficial bacteria and their role in plant growth promotion: a review

Soil beneficial bacteria and their role in plant growth promotion: a review Ann Microbiol (2010) 60:579–598 DOI 10.1007/s13213-010-0117-1 REVIEW ARTICLE Soil beneficial bacteria and their role in plant growth promotion: a review Rifat Hayat & Safdar Ali & Ummay Amara & Rabia Khalid & Iftikhar Ahmed Received: 23 February 2010 /Accepted: 29 July 2010 /Published online: 28 August 2010 Springer-Verlag and the University of Milan 2010 Abstract Soil bacteria are very important in biogeochemical includes the prevention of the deleterious effects of cycles and have been used for crop production for decades. phytopathogenic organisms. This can be achieved by the Plant–bacterial interactions in the rhizosphere are the deter- production of siderophores, i.e. small metal-binding mole- minants of plant health and soil fertility. Free-living soil cules. Biological control of soil-borne plant pathogens and bacteria beneficial to plant growth, usually referred to as plant the synthesis of antibiotics have also been reported in several growth promoting rhizobacteria (PGPR), are capable of bacterial species. Another mechanism by which PGPR can promoting plant growth by colonizing the plant root. PGPR inhibit phytopathogens is the production of hydrogen are also termed plant health promoting rhizobacteria (PHPR) cyanide (HCN) and/or fungal cell wall degrading enzymes, or nodule promoting rhizobacteria (NPR). These are associ- e.g., chitinase and ß-1,3-glucanase. Direct plant growth ated with the rhizosphere, which is an important soil promotion includes symbiotic and non-symbiotic PGPR ecological environment for plant–microbe interactions. Sym- which function through production of plant hormones such biotic nitrogen-fixing bacteria include the cyanobacteria of the as auxins, cytokinins, gibberellins, ethylene and abscisic genera Rhizobium, Bradyrhizobium, Azorhizobium, Allorhi- acid. Production of indole-3-ethanol or indole-3-acetic acid zobium, Sinorhizobium and Mesorhizobium. Free-living (IAA), the compounds belonging to auxins, have been nitrogen-fixing bacteria or associative nitrogen fixers, for reported for several bacterial genera. Some PGPR function example bacteria belonging to the species Azospirillum, as a sink for 1-aminocyclopropane-1-carboxylate (ACC), the Enterobacter, Klebsiella and Pseudomonas,havebeen immediate precursor of ethylene in higher plants, by shown to attach to the root and efficiently colonize root hydrolyzing it into α-ketobutyrate and ammonia, and in this surfaces. PGPR have the potential to contribute to sustain- way promote root growth by lowering indigenous ethylene able plant growth promotion. Generally, PGPR function in levels in the micro-rhizo environment. PGPR also help in three different ways: synthesizing particular compounds for solubilization of mineral phosphates and other nutrients, the plants, facilitating the uptake of certain nutrients from the enhance resistance to stress, stabilize soil aggregates, and soil, and lessening or preventing the plants from diseases. improve soil structure and organic matter content. PGPR Plant growth promotion and development can be facilitated retain more soil organic N, and other nutrients in the plant– both directly and indirectly. Indirect plant growth promotion soil system, thus reducing the need for fertilizer N and P and enhancing release of the nutrients. : : : R. Hayat (*) S. Ali U. Amara R. Khalid Department of Soil Science & SWC, . . . Keywords PGPR Symbiotic Non-symbiotic PMAS Arid Agriculture University, . . P-solubilization Phytohormones Biocontrol Rawalpindi 46300, Pakistan e-mail: hayat@uaar.edu.pk I. Ahmed Introduction Plant Biotechnology Program, National Agricultural Research Centre, Soil bacteria have been used in crop production for Park Road, decades. The main functions of these bacteria (Davison Islamabad, Pakistan 580 Ann Microbiol (2010) 60:579–598 1988) are (1) to supply nutrients to crops; (2) to stimulate fixing bacteria such as Azotobacter, Azospirillum, Bacillus, plant growth, e.g., through the production of plant and Klebsiella sp. are also used to inoculate a large area of hormones; (3) to control or inhibit the activity of plant arable land in the world with the aim of enhancing plant pathogens; (4) to improve soil structure; and (5) bioaccu- productivity (Lynch 1983). In addition, phosphate- mulation or microbial leaching of inorganics (Brierley solubilizing bacteria such as species of Bacillus and 1985; Ehrlich 1990). More recently, bacteria have also Paenibacillus (formerly Bacillus) have been applied to been used in soil for the mineralization of organic soils to specifically enhance the phosphorus status of plants pollutants, i.e. bioremediation of polluted soils (Middledrop (Brown 1974). et al. 1990; Burd et al. 2000; Zhuang et al 2007; Zaidi et al. PGPR have the potential to contribute in the develop- 2008). In the era of sustainable crop production, the plant– ment of sustainable agricultural systems (Schippers et al. microbe interactions in the rhizosphere play a pivotal role 1995). Generally, PGPR function in three different ways in transformation, mobilization, solubilization, etc. of (Glick 1995, 2001): synthesizing particular compounds for nutrients from a limited nutrient pool, and subsequently the plants (Dobbelaere et al. 2003; Zahir et al. 2004), uptake of essential nutrients by plants to realize their full facilitating the uptake of certain nutrients from the soil genetic potential. At present, the use of biological (Lucas et al. 2004a, b; Çakmakçi et al. 2006), and lessening approaches is becoming more popular as an additive to or preventing the plants from diseases (Guo et al. 2004; chemical fertilizers for improving crop yield in an integrat- Jetiyanon and Kloepper 2002; Raj et al. 2003; Saravana- ed plant nutrient management system. In this regard, the use kumar et al. 2008). The mechanisms of PGPR-mediated of PGPR has found a potential role in developing enhancement of plant growth and yield of many crops are sustainable systems in crop production (Sturz et al. 2000; not yet fully understood (Dey et al. 2004). However, the Shoebitz et al. 2009). A variety of symbiotic (Rhizobium possible expalination include (1) the ability to produce a sp.) and non-symbiotic bacteria (Azotobacter, Azospirillum, vital enzyme, 1-aminocyclopropane-1-carboxylate (ACC) Bacillus, and Klebsiella sp., etc.) are now being used deaminase to reduce the level of ethylene in the root of worldwide with the aim of enhancing plant productivity developing plants thereby increasing the root length and (Burd et al. 2000; Cocking 2003). growth (Li et al. 2000; Penrose and Glick 2001); (2) the Free-living soil bacteria beneficial to plant growth are ability to produce hormones like auxin, i.e indole acetic usually referred to as plant growth promoting rhizobacteria acid (IAA) (Patten and Glick 2002), abscisic acid (ABA) (PGPR), capable of promoting plant growth by colonizing (Dangar and Basu 1987; Dobbelaere et al. 2003), gibber- the plant root (Kloepper and Schroth 1978; Kloepper et al. ellic acid (GA) and cytokinins (Dey et al. 2004); (3) a 1989; Cleyet-Marcel et al. 2001). PGPR are also termed as symbiotic nitrogen fixation (Kennedy et al. 1997, 2004); (4) plant health promoting rhizobacteria (PHPR) or nodule antagonism against phytophatogenic bacteria by producing promoting rhizobacteria (NPR) and are associated with the siderophores, ß-1, 3-glucanase, chitinases, antibiotic, fluo- rhizosphere which is an important soil ecological environ- rescent pigment and cyanide (Cattelan et al. 1999; Pal et al. ment for plant–microbe interactions (Burr and Caesar 2001; Glick and Pasternak 2003); (5) solubilization and 1984). According to their relationship with the plants, mineralization of nutrients, particularly mineral phosphates PGPR can be divided into two groups: symbiotic bacteria (de Freitas et al. 1997; Richardson 2001; Banerjee and and free-living rhizobacteria (Khan 2005). PGPR can also Yasmin 2002); (6) enhanced resistance to drought (Alvarez be divided into two groups according to their residing sites: et al. 1996), salinity, waterlogging (Saleem et al. 2007) and iPGPR (i.e., symbiotic bacteria), which live inside the plant oxidative stress (Stajner et al. 1995, 1997); and (7) cells, produce nodules, and are localized inside the production of water-soluble B group vitamins niacin, pan- specialized structures; and ePGPR (i.e., free-living rhizo- tothenic acid, thiamine, riboflavine and biotin (Martinez- bacteria), which live outside the plant cells and do not Toledo et al. 1996;Sierra et al. 1999; Revillas et al. 2000). produce nodules, but still prompt plant growth (Gray and The application of PGPR has also been extended to Smith 2005). The best-known iPGPR are Rhizobia, which remediate contaminated soils in association with plants produce nodules in leguminous plants. A variety of bacteria (Zhuang et al. 2007). Thus, it is an important need to have been used as soil inoculants intended to improve the enhance the efficiency of meager amounts of external inputs supply of nutrients to crop plants. Species of Rhizobium by employing the best combinations of beneficial bacteria in (Rhizobium, Mesorhizobium, Bradyrhizobium, Azorhi- sustainable agriculture production systems. This review zobium, Allorhizobium and Sinorhizobium) have been covers the perspective of soil-beneficial bacteria and the role successfully used worldwide to permit an effective estab- they are playing in plant growth promotion via direct and lishment of the nitrogen-fixing symbiosis with leguminous indirect mechanisims. The further elucidation of different crop plants (Bottomley and Maggard 1990; Bottomley and mechanisms involved will help to make these bacteria a Dughri 1989). On the other hand, non-symbiotic nitrogen- valuable partner in future agriculture. Ann Microbiol (2010) 60:579–598 581 Symbiotic N -fixing bacteria et al. 2003;Hayat 2005; Hayat et al. 2008a, b). In many low input grassland systems, the grasses depend on the N fixed Nitrogen is required for cellular synthesis of enzymes, by the legume counterparts for their N nutrition and protein proteins, chlorophyll, DNA and RNA, and is therefore synthesis, which is much needed for forage quality in important in plant growth and production of food and feed. livestock production (Paynel et al. 2001; Hayat and Ali For nodulating legumes, nitrogen is provided through 2010). In addition to N -fixation in legumes, Rhizobia such symbiotic fixation of atmospheric N by nitrogenase in as species of Rhizobium and Bradyrhizobium produce rhizobial bacteroids. This process of biological nitrogen molecules (auxins, cytokinins, abscicic acids, lumichrome, fixation (BNF) accounts for 65% of the nitrogen currently rhiboflavin, lipochitooligosaccharides and vitamins) that utilized in agriculture, and will continue to be important in promote plant growth (Hardarson 1993; Herridge et al. future sustainable crop production systems (Matiru and 1993; Keating et al. 1998;Hayat andAli 2004; Hayat et al. Dakora 2004). Important biochemical reactions of BNF 2008a, b). Their colonization and infection of roots would occur mainly through symbiotic association of N2-fixing also be expected to increase plant development and grain microorganisms with legumes that converts atmospheric yield (Kloepper and Beauchamp 1992;Dakora 2003; elemental nitrogen (N2) into ammonia (NH3) (Shiferaw et Matiru and Dakora 2004). Other PGPR traits of Rhizobia al. 2004). Rhizobia (species of Rhizobium, Mesorhizobium, and Bradyrhizobia include phytohormone production Bradyrhizobium, Azorhizobium, Allorhizobium and Sino- (Chabot et al. 1996a, b; Arshad and Frankenberger rhizobium) form intimate symbiotic relationships with 1998), siderophore release (Plessner et al. 1993;Jadhav legumes by responding chemotactically to flavonoid mole- et al. 1994), solubilization of inorganic phosphorus (Abd- cules released as signals by the legume host. These plant Alla 1994a;Chabotet al. 1996a) and antagonism against compounds induce the expression of nodulation (nod) genes plant pathogenic microorganisms (Ehteshamul-Haque and in Rhizobia, which in turn produce lipo-chitooligosaccharide Ghaffar 1993). A number of researchers have experimen- (LCO) signals that trigger mitotic cell division in roots, tally demonstrated the ability of Rhizobia to colonize roots leading to nodule formation (Dakora 1995, 2003; Lhuissier of non-legumes and localize themselves internally in tissues, et al. 2001; Matiru and Dakora 2004). Nodules—the sites for including the xylem (Spencer et al. 1994). Applying symbiotic nitrogen fixation—are formed as a result of series Bradyrhizobium japonicum to radish significantly increased of interactions between Rhizobia and leguminous plants. plant dry matter, by 15% (Antoun et al. 1998). Naturally- However, there are number of factors which affect the occurring Rhizobia, isolated from nodules of some tropical nodulation on legume roots including host–microsymbiont legumes, have also been shown to infect roots of many compatibility, physicochemical conditions of the soil and the agricultural species such as rice, wheat and maize via cracks presence of both known and unknown bio-molecules such as made by emerging lateral roots (Webster et al. 1997). In a flavonoides, polysaccharides and hormones (Tisdale et al. study with maize, Chabot et al. (1996b) used biolumines- 1990; Zafar-ul-Hye et al. 2007). It is a molecular dialogue cence from Rhizobium leguminosarum bv. phaseoli strain between the host plant and a compatible strain of Rhizobium harboring lux genes to visualize in situ colonization of roots which serves as an initiate of the development of nodules by Rhizobia, as well as to assess the efficiency with which (Murray et al. 2007). The rhizobial infection begins when the these bacteria infected maize roots. These observations were bacteria enters into roots in a host-controlled manner consistent with findings on maize root colonization and (Limpens et al. 2003). Rhizobium becomes trapped in a infection by Rhizobia reported by Schloter et al. (1997)and cavity formed by curling of root hair. The root hair plasma Yanni et al. (2001). membrane invaginates the cavity, and a tube-like structure is The success of laboratory studies in infected cereal roots formed by which Rhizobium enters the plant and reaches the with Rhizobia led to the hypothesis that during legume– base of the root hair. Consequently, the infection thread reaches cereal rotations and/or mixed intercropping Rhizobia are a nodule primordium in the cortex of the root that develops into brought into closer contact with cereal roots, and this a nodule upon release of the Rhizobium (Limpens et al. 2003). probably results in non-legume root infection by native Sometimes, no nodulation occurs in spite of inoculation with rhizobial populations in the soil. Yanni et al. (1997) certain rhizobial cultures, because the strains used in such isolated Rhizobium leguminosarum bv. trifolii as a natural cases become exopolysaccharide-deficient due to mutation or endophyte from roots of rice in the Nile delta. Because any unspecified reason (van Rhijn et al. 2001). rice has been grown in rotation with berseem clover for Rhizobium–legume symbiosis has been examined exten- about seven centuries in the Nile delta, this probably sively. The N fixed by Rhizobia in legumes can also benefit promoted closer rhizobial affinity to this cereal as a “host associated non-legumes via direct transfer of biologically plant”. This hypothesis is re-enforced by the fact that fixed N to cereals growing in intercrops (Snapp et al. 1998) population of clover-nodulating Rhizobia isolated from rice 7 −1 or to subsequent crops rotated with symbiotic legumes (Shah could occur up to 2.5×10 cell g fresh weight of root, 582 Ann Microbiol (2010) 60:579–598 concentrations similar to those obtained for bacteroids in wheat, maize, sugarcane and cotton), and significantly legume root nodules. Chaintreuil et al. (2000)similarly increase their vegetative growth and grain yield (Kennedy isolated photosynthetic Bradyrhizobia from roots of the et al. 2004). Azotobacter species (Azotobacter vinelandii African brown rice, Oryza glaberrima, which generally and Azotobacter chroococcum) are free-living heterotrophic grows in the same wetland as Aeschynomene sensitiva,a diazotrophs that depend on an adequate supply of reduced stem-nodulated legume associated with photosynthetic strains C compounds such as sugars for their energy source of Bradyrhizobium. Again, this may well suggest co- (Kennedy and Tchan 1992). Their activity in rice culture evolution of Aeschynomene, Bradyrhizobia and wild geno- can be increased by straw application (Kanungo et al. 1997), type of African brown rice. But whether these Bradyrhizobia presumably as a result of microbial breakdown of cellulose affect growth of O. glaberrima plant has not been deter- into cellobiose and glucose. Yield of rice (Yanni and El- mined. Besides rice, Rhizobia have also been isolated as Fattah 1999), cotton (Iruthayaraj 1981; Patil and Patil 1984; natural endophyets from roots of other non-legumes species Anjum et al. 2007), and wheat (Soliman et al. 1995;Hegazi such as cotton, sweet corn (Mclnroy and Kloepper 1995), et al. 1998; Barassi et al. 2000) increased with the maize (Martinez-Romero et al. 2000), wheat (Biederbeck et application of Azotobacter. In contrast to Azotobacter, al. 2000) and canola (Lupwayi et al. 2000) either grown in Clostridia are obligatory anaerobic heterotrophs only capable rotation with legumes or in a mixed cropping system of fixing N in the complete absence of oxygen (Kennedy involving symbiotic legumes. Rhizobial attachment to roots and Tchan 1992; Kennedy et al. 2004). Clostridia can usually of asparagus (Asparagus officinalis L), oat (AvenasativaL.), be isolated from rice soils (Elbadry et al. 1999), and their rice (Oryza sativa), and wheat (Triticum aestivum)has also activity also increased after returning straw to fields, raised been reported by Terouchi and Syono (1990). Wiehe and the C to N ratio in the soil. Holfich (1995) demonstrated that the strain R39 of Rhizobium Beneficial effects of inoculation with Azospirillum on leguminosarum bv. trifolii, multiplied under field conditions wheat yields in both greenhouse and field conditions have in the rhizosphere of host legumes (lupin and pea) as well as been reported (Hegazi et al. 1998; El Mohandes 1999; non-legumes including corn (Zea mays), rape (Brassica napus Ganguly et al. 1999). Strains of Azospirillum, a nitrogen- L) and wheat (Triticum aestivum). The effect of Rhizobium fixing organism living in close association with plants in leguminosarum bv. trifolii on non-legume plant growth has the rhizosphere. Azospirillum species are aerobic hetero- been reported to be similar to Pseudomonas fluorescens as trophs that fix N under microaerobic conditions (Roper PGPR in its colonization on certain plant roots (Hoflich et al. and Ladha 1995) and grow extensively in the rhizosphere 1994; 1995; Hoflich 2000). The plant growth promoting of gramineous plants (Kennedy and Tchan 1992; Kennedy ability of Rhizobia inoculation varies with soil properties and et al. 2004). The Azospirillum–plant association leads to crop rotation (Hilali et al. 2000; 2001). Inoculation response enhancd development and yield of different host plants to Bradyrhizobium largely depends on the soil moisture, (Fallik et al. 1994). This increase in yield is attributed available N, yield potential of the crop, and the abundance mainly to an improvement in root development by an and effectiveness of native Rhizobia (Venkateswarlu et al. increase in water and mineral uptake, and to a lesser extent 1997). In trials conducted in arid areas on legumes like guar biological N -fixation (Okon and Labandera-Gonzalez (Cyamopsis tetragonoloba L. Taub), moth (Vigna acontifolia) 1994; Okon and Itzigsohn 1995). Azospirillum brasilense and mung (Vigna radiata), inoculation gave up to 10–25% shows both chemotaxis and chemokinesis in response to yield benefits with normal rainfall (Rao 2001). Leelahawonge temporal gradient of different chemoeffectors, thereby et al. (2010) isolated root nodule bacteria from the medicinal increasing the chance of root–bacterial interactions. Phyto- legume Indigofera tinctoria and reported a new legume hormones synthesized by Azospirillum influence the host symbiont related to Pseudoalteromonas from the gamma root respiration rate, metabolism and root proliferation and class of proteobactreia. The partial nifHgene of Pseudoalter- hence improve mineral and water uptake in inoculated omonas (strain DASA 57075) had 96% similarity with nifH plants (Okon and Itzigsohn 1995). Azospirillum lipoferum gene of a member of Bradyrhizobium. The partial nodC gene and Azospirillum brasilense have been isolated from roots of Pseudoalteromonas DASA 57075 also had 88% similarity and stems of rice and sugar cane plants (Ladha et al. 1982; with nodC gene of several Rhizobia including Sinorhizobium, James et al. 2000; Reis et al. 2000) while Azospirillum Bradyrhizobium and Mesorhizobium amazonese has been isolated from the roots of rice (Pereira et al. 1988), and root and stems of sugar cane (Reis et al. 2000). In greenhouse studies, inoculation with Azospirillum −1 Non-symbiotic N -fixing bacteria lipoferum increased rice yield up to 6.7 g plant (Mirza et al. 2000). Balandreau (2002) found in a field experiment −1 A range of plant growth promoting rhizobacteria (PGPR) that estimated yield increased was around 1.8 t ha due to participate in interaction with C3 and C4 plants (e.g., rice, inoculation with Azospirillum lipoferum. Wheat grain yield Ann Microbiol (2010) 60:579–598 583 −1 was increased by up to 30% (Okon and Labandera-Gonzalez found capable of saving 25–30 kgN ha of fertilizer. The 1994) by inoculation with Azospirillum brasilense. Plant species B. glumae causes grain and seedling rot of rice inoculation with Azospirillum brasilense promoted greater (Nakata 2002). Another species, B. cepacia, can be hazard- 3- + uptake of NO ,K and H PO in corn, sorghum and wheat ous to human health (Balandreau 2002), so appropriate care 2 4 (Zavalin et al. 1998;Saubidetet al. 2000). Inoculation with and risk-reducing techniques should be employed while Azospirillum brasilense significantly increases cotton plant isolating and culturing species of Burkholderia (Kennedy et height and dry matter under greenhouse conditions (Bashan al. 2004). B. brasilensis is an endophyte of roots, stems and 1998). leaves of sugarcane plant while B. tropicalis is confined to its Soil applications with Azospirillum can significantly roots and stems (Reis et al. 2000). There is also evidence that increase cane yield in both plant and ratoon crops in the these organisms can produce substances antagonistic to field (Shankariah and Hunsigi 2001). The PGPR effects nematodes (Meyer et al. 2000). also increase N and P uptake in field trials (Galal et al. Several species of family Enterobacteriaceae include 2000; Panwar and Singh 2000), presumably by stimulating diazotrophs, particularly those isolated from the rhizosphere greater plant root growth. Substantial increases in N uptake of rice. These enteric genera containing some examples of by wheat plants and grain were observed in greenhouse diazotrophs with PGP activity include Klebsiella, Enter- trials with inoculation of Azospirillum brasilense (Islam et obacter, Citrobacter, Pseudomonas and probably several al. 2002). N tracer techniques showed that Azospirillum others yet unidentified (Kennedy et al. 2004). Klebsiella brasilense and Azospirillum lipoferum contributed 7–12% pneumoniae, Enterobacter cloacae, Citrobacter freundii of wheat plant N by BNF (Malik et al. 2002). Inoculation and Pseudomonas putida or Pseudomonas fluorescens are with Azospirillum brasilense significantly increases N also examples of such plant-associated bacteria. Herbaspir- −1 contents of cotton up to 0.91 mg plant (Fayez and Daw illum is an endophyte which colonises sugarcane, rice, 1987). Inoculation with Azospirillum also significantly maize, sorghum and other cereals (James et al. 2000). It can increased N content of sugarcane leaves in greenhouse fix 31–45% of total plant N in rice (30-day-old rice experiments (Muthukumarasamy et al. 1999). Azospirillum seedling) N from the atmosphere (Baldani et al. 2000). is also capable of producing antifungal and antibacterial The estimated N fixation by Herbaspirillum was 33–58 mg −1 compounds, growth regulators and siderophores (Pandey tube under aseptic conditions (Reis et al. 2000). In a and Kumar 1989). Acetobacter (Gluconacetobacter) diaz- greenhouse study, inoculation with Herbaspirillum in- −1 otrophicus is another acid-tolerant endophyte which grows creased rice yield significantly up to 7.5 g plant (Mirza best on sucrose-rich medium (James et al. 1994; Kennedy et al. 2000). These authors quantified BNF by different et al. 2004). Studies confirmed that up to 60–80% of strains of Herbaspirillum in both basmati and super basmati −1 −1 sugarcane plant N (equivalent to over 200 kgN ha year ) rice. The %N (N derived from the atmosphere) values were was derived from BNF and Azospirillum diazotrophicus is 19.5–38.7, and 38.1–58.2 in basmati and super basmati, apparently responsible for much of this BNF (Boddey et al. respectively. Herbaspirillum seropedicae also acts as an 1991). The Acetobacter-sugarcane system has now become endophytic diazotroph of wheat plants (Kennedy and Islam an effective experimental model and the diazotrophic 2001), colonizing wheat roots internally between the cells. character (nif ) is important component of this system Herbaspirillum seropedicae is also found in roots and (Lee et al. 2002). Reinhold-Hurek et al. (1993) studied a stems of sugarcane plant while Herbaspirillum rubrisubal- strain of the endophytic Gram-negative N -fixing bacterium bicans is an obligate endophyte of roots, stems and leaves Azoarcus sp. BH72, originally isolated from Kallar grass (Reis et al. 2000). Herbaspirilla can also colonize maize (Leptochloa fusa Kunth) growing in the saline-sodic soils plants endophytically and fix N , in addition to sugarcane typical of Pakistan. Azoarcus spp. also colonise grasses, and wheat (James et al. 2000). such as rice, in both laboratory and field conditions (Hurek et al. 1994). In rice roots, the zone behind the meristem was most intensively colonized and response of rice roots to Phosphorus-solubilizing bacteria inoculation with Azoarcus sp. BH72 in aseptic system was cultivar-dependent (Reinhold-Hurek et al. 2002). The genus Phosphorus (P) is one of the major essential macronutrients Burkholderia comprises 67 validly published species, with for plant growth and development (Ehrlich 1990). It is −1 several of these including Burkholderia vietnamiensis, B. present at levels of 400–1,200 mgkg of soil. Phosphorus kururiensis, B. tuberum and B. phynatum being capable of exists in two forms in soil, as organic and inorganic fixing N (Estrada-delos Station et al. 2001; Vandamme et phosphates. To convert insoluble phosphates (both organic al. 2002). When B. vietnamiensis was used to inoculate rice and inorganic) compounds in a form accessible to the plant in a field trial, it increased grain yields significantly up to is an important trait for a PGPR in increasing plant yields −1 8tha (Tran Vân et al. 2000). In field trials, this strain was (Igual et al. 2001; Rodríguez et al. 2006). The concentration 584 Ann Microbiol (2010) 60:579–598 of soluble P in soil is usually very low, normally at levels of al. 1991; Rodríguez and Fraga 1999), phytase (Richardson 1 ppm or less (Goldstein 1994). The plant takes up several P and Hadobas 1997), phosphonoacetate hydrolase (McGrath −2 forms but major part is absorbed in the forms of HPO4 or et al. 1998), D-α-glycerophosphatase (Skrary and Cameron −1 H PO . The phenomenon of P fixation and precipitation in 1998) and C-P lyase (Ohtake et al. 1996). Activity of 2 4 soil is generally highly dependent on pH and soil type. various phosphatases in the rhizosphere of maize, barley, Several reports have documented microbial P release from and wheat showed that phosphatase activity was consider- organic P sources (McGrath et al. 1995; Ohtake et al. 1996; able in the inner rhizosphere at acidic and neutral soil pH McGrath et al. 1998; Rodríguez and Fraga 1999). Bacterial (Burns 1983). Soil bacteria expressing a significant level of strains belonging to genera Pseudomonas, Bacillus, Rhizo- acid phosphatases include strains from the genus Rhizobium bium, Burkholderia, Achromobacter, Agrobacterium, Micro- (Abd-Alla 1994a, b), Enterobacter, Serratia, Citrobacter, ccocus, Aerobacter, Flavobacterium and Erwinia have the Proteus and Klebsiella (Thaller et al. 1995a), as well as ability to solubilize insoluble inorganic phosphate (mineral Pseudomonas (Gügi et al. 1991) and Bacillus (Skrary and phosphate) compounds such as tricalcium phosphate, dical- Cameron 1998). Four strains, namely Arthrobacter ureafa- cium phosphate, hydroxyl apatite and rock phosphate ciens, Phyllobacterium myrsinacearum, Rhodococcus (Goldstein 1986; Rodríguez and Fraga 1999; Rodríguez et erythropolis and Delftia sp. have been reported for the first al. 2006). Strains from genera Pseudomonas, Bacillus and time by Chen et al. (2006) as phosphate-solubilizing Rhizobium are among the most powerful phosphate solubil- bacteria (PSB) after confirming their capacity to solubilize izers, while tricalcium phosphate and hydroxyl apatite seem considerable amounts of tricalcium phosphate in the to be more degradable substrates than rock phosphate (Arora medium by secreting organic acids. There are also more and Gaur 1979; Illmer and Schinner 1992;Halder and reports on phosphate solubilization by Rhizobium (Halder et Chakrabarty 1993; Rodríguez and Fraga 1999;Banerjee et al. 1990, 1991;Abd-Alla 1994a, b; Chabot et al. 1996a, b) al. 2006). The production of organic acids especially and the non-symbiotic nitrogen fixer, Azotobacter (Kumar et gluconic acid seems to be the most frequent agent of mineral al. 2001). The efficacy of a strain of Mesorhizobium phosphate solubilization by bacteria such as Pseudomonas mediterraneum to enhance the growth and phosphorous sp., Erwinia herbicola, Pseudomonas cepacia and Burkhol- content in chickpea and barley plants was assessed in a soil deria cepacia (Rodríguez and Fraga 1999). Another organic with and without addition of phosphates in a growth acid identified in strains with phosphate-solubilizing ability chamber (Peix et al. 2001). The results show that strain is 2-ketogluconic acid, which is present in Rhizobium PECA21 was able to mobilize phosphorous efficiently in leguminosarum (Halder et al. 1990), Rhizobium meliloti plants when tricalcium phosphate was added to soil. The (Halder and Chakrabarty 1993), Bacillus firmus (Banik and effectiveness of strains of Rhizobia used in inoculation of a Dey 1982), and other unidentified soil bacteria (Duff and soil should not be based only on their fixation potential, Webley 1959). Strains of Bacillus licheniformis and B. since these bacteria can also increase plant growth by means amyloliquefaciens were found to produce mixtures of lactic, of other mechanisms including the phosphate solubilization isovaleric, isobutyric, and acetic acids. Other organic acids, (Peix et al. 2001). The phosphate-solubilizing activity of such as glycolic acid, oxalic acid, malonic acid, succinic Rhizobium (e.g., Rhizobium/bradyrhizobium), was associated acid, citric acid and propionic acid, have also been identified with the production of 2-ketogluconic acid which was among phosphate solubilizers (Illmer and Schinner 1992; abolished by the addition of NaOH, indicating that the (Banik and Dey 1982;Chen et al. 2006). Goldstein (1994, phosphate-solubilizing activity of this organism was entirely 1995) has proposed that the direct periplasmic oxidation of due to its ability to reduce pH of the medium (Halder and glucose to gluconic acid, and often 2-ketogluconic acid, Chakrabarty 1993). However, detailed biochemical and forms metabolic basis of the mineral phosphate solubilization molecular mechanisms of phosphate solubilization of sym- phenotype in some Gram-negative bacteria. Alternative biotic nodule bacteria need to be investigated. De Freitas et possibilities other than organic acids include the release of al. (1997) isolated 111 strains from plant rhizospheric soil, H to the outer surface in exchange for cation uptake or and a collection of nine bacteria (PGPR) were screened for ATPase which can constitute alternative ways, with the help P-solubilization in vitro. The P-solubilizing isolates were of H translocation, for solubilization of mineral phosphates identified as two Bacillus brevis strains, Bacillus mega- (Rodríguez and Fraga 1999). terium, B. polymyxa, B. sphaericus, B. thuringiensis and Soil also contains a wide range of organic substrates, Xanthomonas maltophilia (PGPR strains R85). In addition, which can be a source of P for plant growth. To make this phosphate (P)-solubilizing bacteria such as Bacillus and form of P available for plant nutrition, it must be Paenibacillus (formerly Bacillus) sp. have been applied to hydrolyzed to inorganic P. Mineralization of most organic soils to enhance the phosphorus status of plant (Van Veen et phosphorous compounds is carried out by means of al. 1997). The beneficial effects of PSB on plant growth enzymes like phosphatase (phosphohydrolases) (Gügi et varied significantly depending on environmental conditions, Ann Microbiol (2010) 60:579–598 585 bacterial strain, host plant and soil conditions (Şahin et al using the broad-host range vector pRK293 (Fraga et al. 2004; Çakmakçietal. 2006). The most common mechanism 2001). An increase in extracellular phosphatase activity of used by microorganisms for solubilizing tri-calcium phos- the recombinant strain was achieved. The ability of plants to phates seems to be acidification of the medium via obtain phosphorus directly from phytate (the primary source biosynthesis and release of a wide variety of organic acids of inositol and the major stored form of phosphate in plant (Rodríguez and Fraga 1999; Igual et al 2001; Goldstein and seeds and pollen) is very limited. However, the growth and Krishnaraj 2007;Goldstein 2007;Delvasto et al. 2008). phosphorus nutrition of Arabidopsis plants supplied with Genetic manipulation of phosphate-solubilizing bacteria phytate was improved significantly when they were geneti- is another way to enhance their ability for plant growth cally transformed with the phytase gene. Thermally stable improvement (Rodríguez and Fraga 1999; Rodríguez et al. phytase genes (phy) from Bacillus sp. DS11 (Kim et al. 2006). This may include cloning gene(s) involved in both 1998)and from Bacillus subtilis VTT E-68013 (Kerovuo et mineral and organic phosphate solubilization, followed by al. 1998) have been cloned. Acid phosphatase/phytase genes their expression in selected rhizobacterial strains (Rodríguez from Escherichia coli (appA and appA2 genes) have also et al. 2006). Several attempts have been made to identify and been isolated and characterized (Golovan et al. 2000; characterize the genes involved for P uptake and its Rodríguez et al. 1999). Neutral phytase genes have been transportation (Rossolini et al. 1998; Shenoy and Kalagudi recently cloned from Bacillus licheniformis (Tye et al. 2002). 2005). Apart from genes, quantitative trait loci (QTL) A phyA gene has been cloned from the FZB45 strain of governing maize and barley yield under P-deficient con- Bacillus amyloliquefaciens isolated from a group of several ditions have also been identified (Kajar and Jensen 1995). Bacillus having plant growth promoting activity (Idriss et al. Goldstein and Liu (1987) were the first to clone a gene 2002). involved in mineral phosphate solubolization from the Gram- negative bacteria Erwinia herbicola. Expression of this gene allowed production of GA in Escherichia coli HB101 and Other mechanisms of plant growth promotion conferred the ability to solubilize hydroxyl apatite. Another type of gene (gabY) involved in GA production and mineral Rhizosphere bacteria may improve the uptake of nutrients to phosphate solubolization was cloned from Pseudomonas plants and/or produce plant growth promoting compounds. cepacia (Babu-Khan et al. 1995). Genes for four major P They also protect plant root surfaces from colonization by metabolic enzymes have been investigated (Valverde et al. pathogenic microbes through direct competitive effects and 1999). The cytosolic GAPDH is coded by the nuclear gene production of antimicrobial agents. These bacteria can GapC, whereas the chloroplastic GAPDH is encoded by the indirectly or directly affect plant growth (Kloepper et al. nuclear genes GapA and GapB. The nuclear GapN encodes 1989;Kloepper 1993, 1994;Glick 1995; Mantelin and the cytosolic GAPDHN. The PGK is coded by nuclear gene Touraine 2004). pgk (Serrano et al. 1993). These cloned genes are an Symbiotic and non-symbiotic bacteria may promote important source of material for genetic manipulation of plant growth directly through production of plant PGPR strains for this trait. Some of them code for acid harmones (Dangar and Basu 1987;Lynch 1990;Arshad phosphatase enzymes that are capable of performing well in and Frankenberger 1991, 1993;Glick 1995;Garcíade soil. For example, acpA gene isolated from Francisella Salamone et al. 2001; Gutiérrez-Mañero et al. 2001; tularensis expresses an acid phosphatase with optimum Persello-Cartieaux et al. 2003; Dobbelaere et al. 2003; activity at pH 6, with a wide range of substrate specificity Vivas et al. 2005) and other PGP activities (Dobbelaere et al. (Reilly et al. 1996). Also, genes encoding nonspecific acid 2003). Plant growth promoting rhizobacteria (PGPR) syn- phosphatases class A (PhoC) and class B (NapA) isolated thesizes and exports phytohormones which are called plant from Morganella morganii are very promising (Thaller et al. growth regulators (PGRs). These PGRs may play regulatory 1994; 1995b). Among rhizobacteria, a gene from Burkhol- role in plant growth and development. PGRs are organic deria cepacia that facilitates phosphatase activity has been substances that influence physiological processes of plants at isolated (Rodríguez et al. 2000). This gene codes for an outer extremely low concentrations (Dobbelaere et al. 2003). membrane protein that enhances synthesis in the absence of Bacteria known to produce PGRs are listed in Table 1. soluble phosphates inthe medium, and could be involved in P There are five classes of well-known PGRs, namely auxins, transport to the cell. Besides, cloning of two nonspecific gibberellins, cytokinins, ethylene and abscisic acid (Zahir et periplasmic acid phosphatase genes (napD and napE) from al. 2004). Much attention has been given on the role of Rhizobium (Sinorhizobium) meliloti has been accomplished phytohormone auxin. The physiologically most active auxin (Deng et al. 1998, 2001). The napA phosphatase gene from in plants is indole-3-acetic acid (IAA), which is known to the soil bacterium Morganella morganii was transferred to stimulate both rapid (e.g., increases in cell elongation) and Burkholderia cepacia IS-16, a strain used as a biofertilizer, long-term (e.g., cell division and differentiation) responses in 586 Ann Microbiol (2010) 60:579–598 Table 1 Production of plant growth regulators (PGRs) by rhizobacteria and crop responses PGPR PGRs Crops Responses Reference Kluyvera ascorbata Siderophores, Canola, Both strains decreased some plant growth Burd et al. SUD 165 indole-3-acetic acid tomato inhibition by heavy metals (nickel, lead, zinc) (2000) Rhizobium leguminosarum Indole-3-acetic acid Rice Inoculation with R. leguminosarum had significant Biswas et al. growth promoting effects on rice seedlings. (2000) Rhizobium leguminosarum Indole-3-acetic acid Rice Growth promoting effects upon inoculation on Dazzo et al. axenically grown rice seedlings were observed (2000) Azotobacter sp. Indole-3-acetic acid Maize Inoculation with strain efficient in IAA production had Zahir et al. significant growth promoting effects on maize seedlings. (2000) Rhizobacterial isolates Auxins Wheat, rice Inoculation with rhizobacterial isolates had significant Khalid et al. growth promoting effects on wheat and rice (2001) Rhizobacteria (unidentified) Indole-3-acetic acid Brassica Significant correlation between auxin production by PGPR Asghar et al. in vitro and growth promotion of inoculated rapeseed (2002) seedlings in the modified jar experiments were observed Rhizobacteria (unidentified) Indole-3-acetic acid Wheat, rice Rhizobacterial strains active in IAA production had Khalid et al. relatively more positive effects on inoculated seedlings. (2001) Pseudomonas fluorescens Siderophores, Groundnut Involvement of ACC deaminase and siderophore production Dey et al. indole-3-acetic acid promoted nodulation and yield of groundnut (2004) Rhizobacteria (Unidentified) Auxin, indole-3-acetic acid, Wheat Strain produced highest amount of auxin in non-sterilized Khalid et al. acetamide soil and caused maximum increase in growth yield (2003, 2004) Azospirillum brasilense Indole-3-acetic acid, Rice All the bacterial strains increased rice grain yield over Thakuria et al. A3, A4, A7, A10, CDJA uninoculated control (2004) Bacillus circulans P2, Bacillus sp. P3,Bacillus magaterium P5, Bacillus. Sp. Psd7 Streptomyces anthocysnicus Pseudomonas aeruginosa Psd5 Pseudomonas pieketti Psd6, Pseudomonas fluorescens MTCC103, Azospirillum lipoferum Wheat Promoted development of wheat root system even under crude Muratova et al. strains 15 oil contamination in pot experiment in growth chamber (2005) Pseudomonas denitrificans Auxin Wheat, All the bacterial strains had been found to increase plant Egamberdiyeva Pseudomonas rathonis maize growth of wheat and maize in pot experiments (2005) -1 Azotobacter sp. Indole-3-acetic acid Sesbenia, Increasing the concentration of tryptophane from 1 mgml Ahmad et al. -1 Pseudomonas sp. mung bean to 5 mgml resulted in decreased growth in both crops (2005) Pseudomonas sp. Indole-3-acetic acid Wheat A combined bio-inoculation of diacetyl-phloreglucinol producing Roesti et al. PGPR and AMF and improved the nutritional quality of wheat grain (2006) Bacillus cereus RC 18, Indole-3-acetic acid Wheat, All bacterial strains were efficient in indole acetic acid (IAA) Çakmakçi et al. Bacillus licheniformis RC08, spinach production and significantly increased growth of wheat and spinach (2007b) Bacillus megaterium RC07, Bacillus subtilis RC11, Bacillus. OSU-142, Bacillus M-13, Pseudomonas putida RC06, Paenibacillus polymyxa RC05 and RC14 Mesorhizobium loti MP6, Chrom-azurol, siderophore Brassica Mesorhizobium loti MP6-coated seeds enhanced seed germination, Chandra et al. (CAS), hydrocyanic acid early vegetative growth and grain yield as compared to control (2007) (HCN), indole-3-acetic acid Pseudomonas tolaasii Siderophores, Brassica PGPR strains protect canola plant against the inhibitory Dell’Amico et al. ACC23, iIndole-3-acetic acid effects of cadmium (2008) Pseudomonas fluorescens ACC9, Alcaligenes sp. ZN4, Mycobacterium sp. ACC14, Bacillus sp. Indole-3-acetic acid Rice The isolate SVPR 30, i.e. strain of Bacillus sp., proved Beneduzi et al. Paenibacillus sp. to be efficient in promoting a significant increase in the (2008) root and shoot parts of rice plants Streptomyces acidiscabies Hydroxamate Cowpea S. acidiscabies promoted cowpea growth under nickel stress Dimkpa et al. E13 siderophores (2008) Ann Microbiol (2010) 60:579–598 587 plants (Cleland 1990; Hagen 1990). IAA is the most germination, root elongation (as well as symbiotic N fixation common and best characterized phytohormone. It has been in leguminous plants) is inhibited (Jackson 1991). It has been estimated that 80% of bacteria isolated from the rhizosphere proposed that many plant growth promoting bacteria may can produce plant growth regulator IAA (Patten and Glick promote plant growth by lowering the levels of ethylene in 1996). In addition to IAA, bacteria such as Paenibacillus plants. This is attributed to the activity of enzyme 1- polymyxa and Azospirilla also release other compounds in aminocyclopropane-1-carboxylate (ACC) deaminase, which the rhizosphere, like indole-3-butyric acid (IBA), Trp and hydrolyzes ACC, the immediate biosynthesis precursor of tryptophol or indole-3-ethanol (TOL) that can indirectly ethylene in plants (Yang and Hoffman 1984). The products of contribute to plant growth promotion (Lebuhn et al. 1997; this hydrolysis, ammonia and αketobutyrate, can be used by El-Khawas and Adachi 1999). Cytokinins are other impor- the bacterium as a source of nitrogen and carbon for growth tant phytohormones usually present in small amounts in (Klee et al. 1991). In this way, the bacterium acts as a sink for biological samples, and their identification and quantification ACC and thus lowers ethylene level in plants, preventing is difficult. Nieto and Frankenberger (1990b)reportedon some of the potentially deleterious consequences of high cytokinin by using bioassays. The most noticeable effect of ethylene concentrations (Glick et al. 1998; Steenhooudt and cytokinin on plants is enhanced cell division: however, root Vanderleyden 2000; Saleem et al. 2007). PGPR with ACC- development and root hair formation is also reported deaminase trait usually give very consistent results in (Frankenberger and Arshad 1995). Plants and plant- improving plant growth and yield, and thus are good associated microorganisms have been found to contain over candidates for bio-fertilizer formulation (Shaharoona et al. 30 growth promoting compounds of the cytokinin group. It 2006a, 2006b). The role of PGPR in production of has been found that as many as 90% of microorganisms phosphataes, β-gluconase, dehydroginase, antibiotic (Hass found in the rhizosphere are capable of releasing cytokinins and Keel 2003) solubilization of mineral phosphates and when cultured in vitro (Barea et al. 1976). Nieto and other nutrients, stabilization of soil aggregates, improved soil Frankenberger (1990a, 1991) studied the effect of the structure and organic matter contents (Miller and Jastrow cytokinin precursor’s adenine (ADE) and isopentyl alcohol 2000) has been recognized. The mechanisms involved have (IA) and cytokinin-producing bacteria Azotobacter chroo- a significant plant growth promoting potential, retaining coccum on the morphology and growth of radish and maize more soil organic N and other nutrients in plant–soil systems, under in vitro, greenhouse and field conditions. They found thus reducing the need of N and P fertilizers (Kennedy et al. improvement in plant growth. A number of articles have 2004) and enhancing the release of nutrients (Lynch 1990; reported that PGPR also produced gibberellins (GAs). Nautiyal et al. 2000; Walsh et al. 2001;Dobbelaere etal. Dobbelaere et al. (2003) reported that over 89 GAs are 2003; Ladha and Reddy 2003). known to date and are numbered GA1 through GA89 in PGPR has also been used to remediate contaminated approximate order of their discovery (Frankenberger and soils (Zhuang et al. 2007; Huang et al. 2004, 2005; Arshad 1995; Arshad and Frankenberger 1998). The most Narasimhan et al. 2003) and mineralize organic compounds widely recognized gibberellin is GA3 (gibberellic acid), the in association with plants (Saleh et al. 2004). The combined most active GA in plants is GA1, which is primarily use of PGPR and specific contaminant-degrading bacteria responsible for stem elongation (Davies 1995). In addition can successfully remove complex contaminants (Huang et abscisic acid (ABA) has also been detected by radio- al. 2005). The application of certain rhizobacteria can immunoassay or TLC in supernatants of Azospirillium and increase the uptake of Ni from soils by changing its phase Rhizobium sp. cultures (Kolb and Martin 1985;Dangar and (Abou-Shanab et al. 2006). Important genera of bacteria Basu 1987; Dobbelaere et al. 2003). Primary role of ABA in used in natural and man-created bioremediation includes stomatal closure is well established, as well as its uptake by Bacillus, Pseudomonads, Methanobacteria, Ralstonia and and transport in plant, its presence in the rhizosphere coud be Deinococcus, etc. (Milton 2007). Rhodobacter can fix extremely important for plant growth under a water-stressed carbon and nitrogen from air to make biodegradable environment, such as is found in arid and semiarid climates plastics (Sasikala and Ramana 1995). Bacteria Ralstonia (Frankenberger and Arshad 1995). metallidurans (Goris et al. 2001)and Deinocococcus Ethylene is synthesized by many and perhaps all species radiodurans (Callegan et al. 2008) can tolerate high levels of bacteria (Primrose 1979). Ethylene is a potent plant of toxic metals and radioactivity, respectively. These growth regulator that affects many aspects of plant growth, bacteria can also be used to clean up pollutants in iron, development, and senescence (Reid 1987). In addition to its copper, silver and uranium mines. Specific bacteria facilitate recognition as a ripening hormone, ethylene promotes the removal of carbon, nitrogen and phosphorus compounds formation of adventious root and root hair, stimulates while others remove toxic metals, aromatic compounds, germination, and breaks dormancy of seeds (Esashi 1991). herbicides, pesticides and xenobiotics in multi-step processes However, if ethylene concentration remains high after involving both aerobic and anaerobic metabolism (Milton 588 Ann Microbiol (2010) 60:579–598 2007). The bacterium Accumulibacter phosphatis has been duced by various bacteria that promote plant growth and responsible for the removal of phosphates (Hesselmann et al. induce systemic resistance in Arabidopsis thaliana). 1999; Zhang et al. 2003). Previous research has shown the practicality of intro- Indirect plant growth promotion includes the preven- ducing PGPR into commercial peat-based substrates for tion of deleterious effects of phytopathogenic organisms vegetable production in order to increase plant vigor, (Schippers et al. 1987; Dobbelaere et al. 2003;Glick and control root diseases and increase yields (Kokalis-Burelle Pasternak 2003). This can be achieved by the production 2003; Kokalis-Burelle et al. 2002a, 2002b, 2003, 2006; of siderophores, i.e. small iron-binding molecules. In Kloepper et al. 2004). Trials conducted on muskmelon soils, iron is found predominately as ferric ions, a form (Cucumis melo) and water melon (Citrullus lanatus) that cannot be directly assimilated by microorganisms. resulted in reduction of root knot nematode disease severity Siderophore production enables bacteria to compete with with several PGPR formulations (Kokalis-Burelle et al. pathogens by removing iron from the environment (O´ 2003). Kokalis-Burelle et al. (2006) conducted field trials in Sullivan and O´Gara 1992;Persello-Cartieauxetal. 2003). Florida on bell pepper (Capsicum annuum) to monitor the Siderophore production is very common among Pseudo- population dynamics of two plant growth-promoting rhizo- monads (O´Sullivan and O´Gara 1992), Frankia (Boyer et bacteria (PGPR) strains (Bacillus subtilis strain GBO3 and al. 1999)and Streptomyces sp. (Loper and Buyer 1991) Bacillus amyloliquefaciens strain IN937a) applied in the have also been shown to produce iron-chelating com- potting media at seedling stage and at various times after pounds. Biological control of soil-borne plant pathogens transplanting to the field during the growing season. Most (Sutton and Peng 1993;Idrissetal. 2002; Chin-A-Woeng treatments reduced disease incidence in a detached leaf et al. 2003;Picardetal. 2004) and the synthesis of assay compared to control, indicating that systemic antibiotics have also been reported in several bacterial resistance was induced by PGPR treatments. Application species (O´Sullivan and O´Gara 1992;Haansuuetal. of PGPR strains did not adversely affect populations of 1999). Another mechanism by which rhizobacteria can beneficial indigenous rhizosphere bacteria including inhibit phytopathogens is the production of hydrogen fluorescent pseudomonads and siderophore-producing cyanide (HCN) and/or fungal cell wall-degrading enzymes bacterial strains. Treatment with PGPR increased pop- e.g., chitinase and ß-1, 3-glucanase (Friedlender et al. 1993; ulations of fungi in the rhizosphere but did not result in Bloemberg and Lugtenberg 2001; Persello-Cartieaux et al. increased root disease incidence. This fungal response to 2003). Although pectinolytic capability is usually associated PGPR products was likely due to an increase in with phytopathogenic bacteria, nonphytopathogenic species nonpathogenic chitinolytic fungal strains resulting from such as Rhizobium (Angle 1986), Azospirillum (Umali- application of chitosan, which is a component of the Garcia et al. 1980;Tienet al. 1981), some strains of PGPR formulation applied to the potting media. Table 2 Klebsiella pneumoniae and Yersinia (Chatterjee et al. 1978), cites important studies of biological control by PGPR and Frankia (Séguin and Lalonde 1989) are also able to against certain diseases, pathogens and insects in different degrade pectin. In general, pectinolytic enzymes play an crops. important role in root invasion by bacteria. While PGPR Inoculation of Pseudomonas fluorescens isolates have been identified within many different bacterial taxa, PGPR1, PGPR2 and PGPR4 reduced the seedling mortality most commercially developed PGPR are species of Bacillus caused by Aspergillus niger (Dey et al. 2004). Inoculation which come from endospores that confer population stability of Pseudomonas fluorescens isolates PGPR4 and PGPR5 during formulation and storage of products. Among bacilli, showed strong inhibition to Sclerotium rolfsii, and reduced strains of Bacillus subtilis are the most widely used PGPR the incidence of stem rot severity. Several Pseudomonas due to their disease-reducing and antibiotic-producing fluorescens isolates, viz. PGPR1, PGPR2 and PGPR4, also capabilities when applied as seed treatments (Brannen and produced siderophores and antifungal metabolites. Produc- Backman 1994; Kokalis-Burelle et al. 2006). Specific tion of antifungal metabolites by fluorescent pseudomonads mechanisms involved in pathogen suppression by PGPR has also been found to suppress soil-borne fungal patho- vary and include antibiotic production, substrate compe- gens on many occasions (Pal et al. 2001; Dey et al. 2004). tition, and induced systemic resistance in the host (Van There are some cases where PGPR promoted plant growth Loon et al. 1998). Flourescent pseudomonads are known in non-sterile soil by controlling fungal diseases (Cattelan et to suppress soil-borne fungal pathogens by producing al. 1999). The addition of siderophores-producing Pseudo- antifungal metabolites and by sequestering iron in the monas putida converted a fusarium-conducive soil into a rhizosphere through release of iron-chelating sidero- fusarium-suppressive soil for growth of different plants phores, and thus rendering it unavailable to other (Dey et al. 2004). Improvement in plant growth and disease organisms (Dwivedi and Johri 2003). Ryu et al. (2004) resistance to a broad array of plant pests can be accom- have identified several volatile organic compounds pro- plished using PGPR (Kloepper et al. 2004). The concept of Ann Microbiol (2010) 60:579–598 589 Table 2 Biological control by PGPR against diseases, pathogens and insects in different crops PGPR Crops Disease/pathogen/insect Reference Bacillus amyloliquefaciens strain 1 N 937a Tomato Tomato mottle virus Murphy et al. (2000) Bacillus subtilis 1 N 937b Pseudomonas fluorescens and Tobacco Tobacco necrosis virus, wild fire Park and Kloepper (2000) unidentified PGPR (Ps. syringae, Pv. tabaci) Pseudomonas aeruginosa, Bacillus subtilis Mung bean Root rot, root knot Siddiqui et al. (2001) Streptomyces marcescens 90-116, Tobacco Blue mold Zhang et al. (2003) Bacillus pumilus SE 34, Pseudomonas fluorescens 89B-61, Bacillus pumilus T4, Bacillus pasteurii C-9 Pseudomonas sp White clover Medicago Blue green aphids Acyrthosiphon kondoi Shinji Kempster et al. (2002) Bacillus sp. Cucumber Cotton aphids Aphiz gossypii Glover Stout et al. (2002) Bacillus amyloliquefaciens Pepper Myzus persicae Kokalis-Burelle et al. (2002b) strain 1 N 937a Bacillus subtilis G803 Pseudomonas sp. Groundnut Charcoal rot caused by Rhizoctonia bataticola Gupta et al. (2002) Azotobacter sp., Pseudomonas sp. Wheat Fungal biocontrol Wachowaska (2004) Bacillus licheniformis Tomato, pepper Myzus persicae Lucas et al. (2004b) Pseudomonas fluorescens Pea nut Collar rot caused by Aspergillus niger, Aspergillus flavus Dey et al. (2004) and stem rot caused by Sclerotium rolfsii Glomus mosseae, Bacillus subtilis, Strawberry Crown rot caused by Phytophothora cactorum and Vestberg et al. (2004) Pseudomonas fluorescens red steel caused by Phytophothora fragari Trichoderma harzianum, Gliocladium catenalatum Bacillus cereus MJ-1 Red pepper Myzus persicae Joo et al. (2005) Paenibacillus polymyxa E681 Sesame Fungal disease Ryu et al. (2006) Mesorhizobium loti MP6, Mustard Brassica compestris White rot Sclerotinia sclerotiorum Chandra et al. (2007) Bacillus amyloliquoefaciens, Bell pepper Green peach aphids, Myzus persicae Sluzer Herman et al. (2008) Bacillus subtilis Azospirillum brasilense Sp245 Prunus cerasifera L. clone Mr. 2/5 Rhizosphere fungi Russo et al. (2008) Rhizoctonia sp. Bacillus cereus BS 03, Pigeonpea Fusarial wilt, Fusarium udum Dutta et al. (2008) Pseudomonas aeruginosa RRLJ04 Rhizobia Pseudomonadaceae family. Pea, entil and chickpea Pythium sp. Hynes et al. (2008) Fusarium avenaceum Enterobacteriaceae family Rhizoctonia solani CKP7 introducing PGPR into the rhizosphere using the transplant establishment and disease (Dwivedi and Johri 2003). plug is based on the hypothesis that their establishment in Because typical disease control levels observed with the relatively clean environment of planting media would PGPR are less than those achieved with chemicals, it is afford them an opportunity to develop stable populations in feasible to utilize PGPR as components in integrated the seedling rhiozosphere, and that these populations would management systems that include reduced rates of chem- then persist in the field. It was also hypothesized that early icals and cultural control practices (Kokalis-Burelle et al. exposure to PGPR might precondition young plants to 2006). Attempts to identify methyl bromide, a soil resist pathogen attack after transplanting in the field. It is fumigant alternative for vegetable production, has led to well recognized that PGPR can influence plant growth and re-examination of existing soil fumigants (Gilreath et al. resistance to pathogens (Cleyet-Marcel et al. 2001). 2001), such as 1,3-D, metam sodium and chloropicrin, and However, it is necessary to establish a greater under- development of new broad-spectrum biocides, such as standing of the dynamics of applied beneficial organisms methyl iodide and propargyl bromide (Ohr et al. 1996; under field conditions in order to optimize their applica- Noling and Gilreath 2001), as well as increasing interest in tion method and timing. It is also important to under- non-chemical approaches. PGPR have attracted much stand the effects of applied biocontrol strains on attention in their role in reducing plant diseases. Although populations of indigenous beneficial bacteria including their full potential has not yet been reached, the work to fluorescent pseudomonads, which commonly occur in the date is very promising. Some PGPR, especially if they are rhizosphere, and are known to suppress pathogen inoculated on seeds before planting, are able to establish 590 Ann Microbiol (2010) 60:579–598 themselves on crop roots. They use scarce resources, and Abou-Shanab RAI, Angle JS, Chaney RL (2006) Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate thereby prevent or limit the growth of pathogenic micro- and high Ni soils. Soil Biol Biochem 38:2882–2889 organisms. This is a common way in which PGPR reduce Ahmad F, Ahmad I, Khan MS (2005) Indole acetic acid production the severity of damping-off (Pythium ultimum)inmany by the indigenous isolates of Azotobacter and Flourescent crops. Even if nutrients are not limiting, establishment of pseudomonas in the presence and absence of tryptophan. Turk J Biol 29:29–34 beneficial organisms on roots limits the chance that a Alvarez MI, Sueldo RJ, Barassi CA (1996) Effect of Azospirillum on pathogenic organism that arrives later will find space to coleoptile growth in wheat seedlings under water stress. Cereal become established. Numerous rhizosphere organisms are Res Commun 24:101–107 Angle JS (1986) Pectic and proteolytic enzymes produced by fast- capable of producing compounds that are toxic to and slow-growing soybean Rhizobia. Soil Biol Biochem pathogens (plant diseases). Bacillus subtilis is one such 18:115–116 commercialized PGPR organism, and it acts against a Anjum MA, Sajjad MR, Akhtar N, Qureshi MA, Iqbal A, Jami AR, wide variety of pathogenic fungi (Banerjee et al. 2006). Hassan M (2007) Response of cotton to plant growth promoting rhizobacteria (PGPR) inoculation under different levels of nitrogen. J Agric Res 45(2):135–143 Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Conclusion Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on Soil bacteria transform atmospheric N into ammonia and are radishes (Raphanus sativus L). Plant Soil 204:57–68 Arora P, Gaur AC (1979) Microbial solubilization of different central to soil and plant health. They play a pivotal role in inorganic phosphates. Indian J Exp Biol 17:1258–1261 cycling of nutrients within the soil. The soil contains Arshad M, Frankenberger WT Jr (1991) Effects of soil properties and numerous genera of bacteria, many of which not only have trace elements on ethylene production in soils. Soil Sci 151:377– important roles in nutrient cycling but also protect crops 386 Arshad M, Frenkenberger WT Jr (1993) Microbial production of plant against diseases. Plant growth promoting rhizobacteria growth regulators. In: Meeting FB Jr (ed) Soil microbial ecology. (PGPR) benefit the growth and development of plants Dekker, New York, pp 307–347 directly and indirectly through several mechanisms. The Arshad M, Frankenberger WT Jr (1998) Plant growth regulating production of secondary metabolites, i.e. plant growth substances in the rhizosphere. Microbial production and function. Adv Agron 62:46–51 substances, changes root morphology resulting in greater Asghar HN, Zahir ZA, Arshad M, Khaliq A (2002) Relationship root surface area for the uptake of nutrients, siderophores between in vitro production of auxins by rhizobacteria and their production, antagonism to soil-borne root pathogens, phos- growth-promoting activities in brassica junceal. Biol Fertil Soils 35(23):1–237 phate solubilization, and di-nitrogen fixation. The root Babu-Khan S, Yeo C, Martin WL, Duron MR, Rogers R, Goldstein A surface area for uptake of nutrients and production of PGPR (1995) Cloning of a mineral phosphate-solubilizing gene from may help to optimize nutrient cycling in the event of stresses Pseudomonas cepacia. Appl Environ Microbiol 61:972–978 due to unsuitable weather or soil conditions. Biological Balandreau J (2002) The spermosphere model to select for plant inoculums for legumes have attracted much attention growth promoting rhizobacteria. In: Kennedy IR, Choudhury ATMA (eds) Biofertilisers in action. Rural Industries Research throughout the world. Other PGPR inoculants (Azospirillum, and Development Corporation, Canberra, pp 55–63 Azotobacter, Bacillus, Pseudomonas, etc.) are also available Baldani VLD, Baldani JI, Dobereiner J (2000) Inoculation of rice plants for a variety of crops, used alone or co-inoculating with with the endophytic diazotrophs Herbaspirillums seropidicae.Biol Rhizobium sp. These technologies have resulted in positive Fertil Soils 30:485–491 Banerjee MR, Yasmin L (2002) Sulfur oxidizing rhizobacteria: an responses under controlled (laboratory and greenhouse) innovative environment friendly soil biotechnological tool for conditions; however, natural variations make it difficult to better canola production. Proceeding of AGROENVIRON. predict how PGPR may respond when applied to field Cairo, Egypt, 2002, October 26–29, pp 1-7 conditions. PGPR must be propagated artificially to optimize Banerjee MR, Yesmin L, Vessey JK (2006) Plant growth promoting rhizobacteria as biofertilizers and biopesticides. In: Rai MK (ed) their viability and biological activity under field applications. Handbook of microbial biofertilizers. Haworth Press, New York It is also suggested that PGPR need to be reinoculated every Banik S, Dey BK (1982) Available phosphate content of an alluvial year/season as they will not live forever in the soil. soil is influenced by inoculation of some isolated phosphate- solubilizing microorganisms. Plant Soil 69:353–364 Barassi CA, Creus CM, Casanovas EM, Sueldo RJ (2000) Could Azospirillum mitigate abiotic stress effects in plants? Auburn University. Web site: http://www.ag.auburn.edu/argentina/ References pdfmanuscripts/brassi.pdf Barea JM, Navarro E, Montoya E (1976) Production of plant growth Abd-Alla MH (1994a) Solubilization of rock phosphates by regulators by rhizosphere phosphate solubilizing bacteria. J Appl Rhizobium and Bradyrhizobium. Folia Microbiol 39:53–56 Bacteriol 40:129–134 Abd-Alla MH (1994b) Use of organic phosphorus by Rhizobium Bashan Y (1998) Azospirillum plant growth-promoting strains are leguminosarum biovar. viceae phosphatases. Biol Fertil Soils nonpathogenic on tomato, pepper, cotton, and wheat. Can J 18:216–218 Microbiol 44:168–174 Ann Microbiol (2010) 60:579–598 591 Beneduzi A, Peres D, Vargas LK, Bodanese-Zanettini MH, Passaglia Chabot R, Antoun H, Kloepper JW, Beauchamp CJ (1996b) Root LMP (2008) Evaluation of genetic diversity and plant growth colonization of maize and lettuce by bioluminescent Rhizobium promoting activities of nitrogen-fixing Bacilli isolated from rice leguminosaurm biovar phaseoli. Appl Environ Microbiol fields in South Brazil. Appl Soil Ecol 39:311–320 62:2767–2772 Biederbeck VO, Lupwayi NZ, Haanson KG, Rice WA, Zentner RP Chaintreuil C, Giraud E, Prin Y, Lorquin J, Ba A, Gillis M, deLajudie (2000) Effect of long-term rotation with lentis on rhizosphere P, Dreyfus B (2000) Photosynthetic bradyRhizobia are natural ecology and on endophytic Rhizobia in wheat. Abstract of the endophytes of the African wild rice Oryza breviligulata. Appl 17th North American Conference on Symbiotic Nitrogen Environ Microbiol 66:5437–5447 Fixation. Laval University Quebec, Canada, pp 23–28, July 2000 Chandra S, Choure K, Dubey RC, Maheshwari DK (2007) Rhizosphere Biswas JC, Ladha JK, Dazzo FB, Yanni YG, Rolf BG (2000) competent Mesorhizobium loti MP6 induces root hair curling, Rhizobial inoculation influences seedling vigor and yield of rice. inhibits Sclerotinia sclerotiorum and enhances growth of Indian Agron J 90:880–886 mustard (Brassica campestris). Braz J Microbiol 38:124–130 Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant Chatterjee AK, Buchanan GE, Behrens MK, Starr MP (1978) growth promotion and biocontrol by rhizobacteria. Curr Opin Synthesis and excretion of polygaracturonic and transeliminase Plant Biol 4:343–350 in Erwinia, Yersinia, and Klebsiella species. Can J Microbiol Boddey RM, Urquiaga S, Reis V, Döbereiner J (1991) Biological nitrogen 25:94–102 fixation associated with sugar cane. Plant Soil 137:111–117 Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Bottomley PJ, Dughri MH (1989) Population size and distribution of Phosphate solubilizing bacteria from subtropical soil and their Rhizobium leguminosarum biovar trifolii in relation to total soil tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41 bacteria and soil depth. Appl Environ Microbiol 55:959–964 Chin-A-Woeng TFC, Bloemberg GV, Lugtenberg BJJ (2003) Phenazines Bottomley PJ, Maggard SP (1990) Determination of viability within and their role in biocontrol by Pseudomonas bacteria. New Phytol serotypes of a soil population of Rhizobium leguminosarum 157:503–523 biovar trifolii. Appl Environ Microbiol 56:533–540 Cleland RE (1990) Auxin and cell elongation. In: Davies PJ (ed) Plant Boyer GL, Kane SA, Alexander JA, Aronson DB (1999) Siderophore hormones and their role in plant growth and development. formation in iron-limited cultures of Frankia sp. strain 52065 and Kluwer, Dordrecht, pp 132–148 Frankia sp. strain CeSI5. Can J Bot 77:1316–1320 Cleyet-Marcel JC, Larcher M, Bertrand H, Rapior S, Pinochet X (2001) Brannen PM, Backman PA (1994) Suppression of Fusarium wilt of Plant growth enhancement by rhizobacteria. In: MorotGaudry JF cotton with Bacillus subtilis hopper box formulations. In: Ryder (ed) Nitrogen assimilation by plants: physiological, biochemicval MH, Stephens PM, Bowen GD (eds) Improving plant productivity and molecular aspects. Science Publishers, Plymouth, pp 185–197 with rhizosphere bacteria, proceedings from the third international Cocking EC (2003) Endophytic colonization of plant roots by workshop on plant growth-promoting rhizobacteria. CSIRO Press, nitrogen-fixing bacteria. Plant Soil 252(1):169–175 Adelaide, pp 83–85 Dakora FD (1995) Plant flavonoids: biological molecules for useful Brierley JA (1985) Use of microorganisms for mining metals. In: exploitation. Aust J Plant Physiol 22:7–99 Halvorson HO, Pramer D, Rogul M (eds) Engineered organisims Dakora FD (2003) Defining new roles for plant and rhizobial in the environment: scientifc issues. ASM Press, Washington, pp molecules in sole and mixed plant cultures involving symbiotic 141–146 legumes. New Phytol 158:39–49 Brown ME (1974) Seed and root bacterization. Annu Rev Phytopathol Dangar TK, Basu PS (1987) Studies on plant growth substances, 12:181–197 IAA metabolism and nitrogenase activity in root nodules of Burd G, Dixon DG, Glick BR (2000) Plant growth promoting bacteria Phaseolus aureus Roxb. var. mungo. Biol Plant 29:350–354 that decrease heavy metal toxicity in plants. Can J Microbiol Davies PJ (1995) The plant hormones: their nature, occurrence, and 46:237–245 functions. In: Davies PJ (ed) Plant hormones: physiology, biochem- Burns RG (1983) Extracellular enzyme-substrate interactions in istry, and molecular biology, 2nd edn. Kluwer, Dordrecht, pp 1–12 soil. In: Slater JH, Whittenbury R, Wimpenny JWT (eds) Davison J (1988) Plant beneficial bacteria. Biotechnology 6:282–286 Microbes in their natural environment. Cambridge University Dazzo FB, Yanni YG, Rizk R, De Bruijn FJ, Rademaker J, Squartini A, Press, Cambridge, pp 249–298 Corich V, Mateos P, Martinez-Molina E et al (2000) Progress in Burr TJ, Caesar A (1984) Beneficial plant bacteria. Crit Rev Plant Sci multinational collaborative studies on the beneficial association 2:1–20 between Rhizobium Ieguminosarum by trifolii and rice. In: Ladha Çakmakçi R, Dönmez F, AydınA, Şahin F (2006) Growth promotion of JK, Reddy PM (eds) The quest for nitrogen fixation in rice. IRR1, plants by plant growth-promoting rhizobacteria under greenhouse Los Banos, Philippines, pp 167–189 and two different field soil conditions. Soil Biol Biochem 38:1482– De Freitas JR, Banerjee MR, Germida JJ (1997) Phosphate- 1487 solubilizing rhizobacteria enhance the growth and yield but not Çakmakçi R, Erat M, Erdoğan ÜG, Dönmez MF (2007) The influence phosphorus uptake of canola (Brassica napus L.). Biol Fertil of PGPR on growth parameters, antioxidant and pentose Soils 24:358–364 phosphate oxidative cycle enzymes in wheat and spinach plants. Dell’Amico E, Cavalca L, Andreoni V (2008) Improvement of J Plant Nutr Soil Sci 170:288–295 Brassica napus growth under cadmium stress by cadmium- Callegan RP, Nobre MF, McTernan PM, John BR, Navarro-González resistant rhizobacteria. Soil Biol Biochem 40:74–84 R, McKay CP, da Costa MS, Rainey FA (2008) Description of Delvasto P, Valverde A, Ballester A, Muñoz JA, González F, Blázquez four novel psychrophilic, ionizing radiation-sensitive Deinococ- ML, Igual JM, García-Balboa C (2008) Diversity and activity of cus species from alpine environments. Int J Syst Evol Microbiol phosphate bioleaching bacteria from a high-phosphorus iron ore. 58:1252–1258 Hydrometallurgy 92:124–129 Cattelan AJ, Hartel PG, Fuhrmann JJ (1999) Screening for plant Deng S, Summers ML, Kahn ML, McDermontt TR (1998) Cloning growth rhizobacteria to promote early soybean growth. Soil Sci and characterization of a Rhizobium meliloti nonspecific acid Soc Am J 63:1670–1680 phosphatase. Arch Microbiol 170:18–26 Chabot R, Antoun H, Cescas MP (1996a) Growth promotion of maize Deng S, Elkins JG, Da LH, Botero LM, McDermott TR (2001) Cloning and lettuce by phosphate-solubilizing Rhizobium leguminosarum and characterization of a second acid phosphatase from Sinorhizobium biovar phaseoli. Plant Soil 184:311–321 meliloti strain 104A14. Arch Microbiol 176:255–263 592 Ann Microbiol (2010) 60:579–598 Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion fibre-legume-cereal system in an Aeric haplaquept. Indian J Agric and yield enhancement of peanut (Arachis hypogaea L) by Res 33:35–39 application of plant growth promoting rhizobacteria. Microbiol García de Salamone IE, Hynes RK, Nelson LM (2001) Cytokinin Res 159:371–394 production by plant growthpromoting rhizobacteria and selected Dimkpa C, Aleš S, Dirk M, Georg B, Erika K (2008) Hydroxamate mutants. Can J Microbiol 47(5):404–411 siderophores produced by Streptomyces acidiscabies E13 bind Gilreath JP, Noling JW, Mirusso J, Nance J, Eger J, Gilreath P (2001) nickel and promote growth in cowpea (Vigna unguiculata L.) Telone and herbicides: do's, don’ts, and maybe's-a primer for under nickel stress. Can J Microb 54:163–172 tomorrow's farmer. FACTS Proceedings of the IFAS, University Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth- of Florida, pp 37-40 promoting effects of diazotrophs in the rhizosphere. Crit Rev Glick BR (1995) The enhancement of plant growth by free-living Plant Sci 22:107–149 bacteria. Can J Microbiol 41:109–117 Duff RB, Webley DM (1959) 2-Ketogluconic acid as a natural Glick BR (2001) Phytoremediation: synergistic use of plants and chelator produced by soil bacteria. Chem Ind 1376-1377 bacteria to cleanup the environment. Biotechnol Adv 21(3):83– Dutta S, Mishra AK, Kuma BSD (2008) Induction of systemic 393 resistance against fusarial wilt in pigeon pea through interaction Glick BR, Pasternak JJ (2003) Plant growth promoting bacteria. In: of plant growth promoting rhizobacteria and rhizobia. Soil Biol Glick BR, Pasternak JJ (eds) Molecular biotechnology principles Biochem 40:452–461 and applications of recombinant DNA, 3rd edn. ASM Press, Dwivedi D, Johri BN (2003) Antifungals from fluorescent pseudomonads: Washington, pp 436–454 biosynthesis and regulation. Curr Sci 12:1693–1703 Glick BR, Penrose DM, Li J (1998) A model for lowering plant Egamberdiyeva D (2005) Plant growth promoting rhizobacteria ethylene concentration by plant growth promoting rhizobacteria. isolated from a calsisol in semi arid region of Uzbekistan: J Theor Biol 190:63–68 biochemical characterization and effectiveness. J Plant Nutr Soil Goldstein AH (1986) Bacterial solubilization of microbial phosphates: Sci 168:94–99 a historical perspective and future prospects. Am J Altern Agric Ehrlich HL (1990) Geomicrobiology, 2nd edn. Dekker, New York, p 646 1:51–57 Ehteshamul-Haque S, Ghaffar A (1993) Use of Rhizobia in the control Goldstein AH (1994) Involvement of the quinoprotein glucose of root diseases of sunflower, okra, soybean and mungbean. J dehydrogenase in the solubilization of exogenous mineral Phytopathol 138:157–163 phosphates by Gram negative bacteria. In: Torriani-Gorni A, Elbadry M, El-Bassel A, Elbanna K (1999) Occurrence and dynamics Yagil E, Silver S (eds) Phosphate in microorganisms: cellular and of phototrophic purple nonsulphur bacteria compared with other molecular biology. ASM Press, Washington, pp 197–203 asymbiotic nitrogen fixers in rice fields of Egypt. World J Goldstein AH (1995) Recent progress in understanding the molecular Microbiol Biotechnol 15:359–362 genetics and biochemistry of calcium phosphate solubilization by El-Khawas H, Adachi K (1999) Identification and quantification of Gram negative bacteria. Biol Agric Hortic 12:185–193 auxins in culture media of Azospirillum and Klebsiella and their Goldstein AH (2007) Future trends in research on microbial phosphate effect on rice roots. Biol Fertil Soils 28:377–381 solubilization: one hundred years of insolubility. In: Velázquez E, El Mohandes MAO (1999) The use of associative diazotrophs with Rodríguez-Barrueco C (eds) First international meeting on microbial different rates of nitrogen fertilization and compost to enhance phosphate solubilization. Springer, Dordrecht, pp 91–96 growth and N -fixation of wheat. Bulletin of Faculty of Goldstein AH, Liu ST (1987) Molecular cloning and regulation of a Agriculture, University of Cairo 50:729-753 mineral phosphate solubilizing gene from Erwinia herbicola. Esashi Y (1991) Ethylene and seed germination. In: Matoo AK, Suttle Biotechnology 5:72–74 JC (eds) The plant hormone ethylene. CRC Press, Boca Raton, Goldstein AH, Krishnaraj PU (2007) Phosphate solubilizing pp 133–157 microorganisms vs. phosphate mobilizing microorganisms: Estrada-delos Station P, Bustitio-Cristales R, Caballero-Mallado J what separates a phenotype from a trait? In: Velázquez E, (2001) Burkholderia, a genus rich in plant-associated nitrogen Rodríguez-Barrueco C (eds) First International meeting on fixers with wide environmental and geographic distribution. Appl microbial phosphate solubilization. Springer, Dordrecht, pp Environ Microbiol 67:279–2798 203–213 Fallik E, Sarig S, Okon Y (1994) Morphology and physiology of plant Golovan S, Wang G, Zhang J, Forsberg CW (2000) Characterization roots associated with Azospirillum. In: Okon Y (ed) and over production of the Escherichia coli appA encoded Azospirillum-plant associations. CRC Press, Boca Raton, pp bifunctional enzyme that exhibits both phytase and acid 77–84 phosphatase activities. Can J Microbiol 46:59–71 Fayez M, Daw ZY (1987) Effect of inoculation with different strains Goris J, De Vos P, Coenye T, Hoste B, Janssens D, Brim H, Diels L, of Azospirillum brasilense on cotton (Gossypium barbadense). Mergeay M, Kersters K, Vandamme P (2001) Classification of Biol Fertil Soils 4(9):1–95 metal-resistant bacteria from industrial biotopes as Ralstonia Fraga R, Rodríguez H, Gonzalez T (2001) Transfer of the gene campinensis sp. nov., Ralstonia metallidurans sp. nov and encoding the Nap A acid phosphatase from Morganella morganii Ralstonia basilensis. Int J Syst Evol Microbiol 51:1773–1782 to a Burkholderia cepacia strain. Acta Biotechnol 21:359–369 Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: Frankenberger WTJ, Arshad M (1995) Photohormones in soil: commonalities and distinctions in the plant-bacterium signaling microbial production and function. Dekker, New York, p 503 processes. Soil Biol Biochem 37:395–412 Friedlander AM, Welkos SL, Pitt MLM, Ezzell JW, Worsham PL, Gügi B, Orange N, Hellio F, Burini JF, Guillou C, Leriche F, Guespin- Rose KJ (1993) Postexposure prophylaxis against experimental Michel JF (1991) Effect of growth temperature on several inhalation anthrax. J Infect Dis 167:1239–1242 exported enzyme activities in the psychrotropic bacterium Galal YGM, El-Ghandour IA, Aly SS, Soliman S, Gadalla A (2000) Pseudomonas fluorescens. J Bacteriol 173:3814–3820 Non-isotopic method for the quantification of biological nitrogen Guo JH, Qi HY, Guo YH, Ge HL, Gong LY, Zhang LX (2004) Biocontrol fixation and wheat production under field conditions. Biol Fertil of tomato wilt by plant growth promoting rhizobacteria. Biol Soils 32:47–51 Control 29:66–72 Ganguly TK, Jana AK, Moitra DN (1999) An evaluation of agronomic Gupta CP, Dubey RC, Maheshwari DK (2002) Plant growth potential of Azospirillum brasilense and Bacillus megaterium in enhancement and suppression of Macrophomina phaseolina Ann Microbiol (2010) 60:579–598 593 causing charcoal rot of peanut by fluorescent Pseudomonas. Biol Bell CR, Brylinsky M, Johnson-Green P (eds) Proceedings of the Fertl Soil 35:295–301 8th international symposium on microbial ecology. Atlantic Gutiérrez-Mañero FG, Ramos-solano B, Probanza A, Mehouachi J, Canada Soc, Microbial Ecol., Halifax, Canada, pp 827-830 Tadeo FR, Talon M (2001) The plant-growth promoting Hoflich G, Wiehe W, Kohn G (1994) Plant growth stimulation by rhizobacteria Bacillus pumilus and Bacillus licheniformis inoculation with symbiotic and associative rhizosphere micro- produce high amounts of physiologically active gibberellins. organisms. Experienca 50:897–905 Physiol Plant 111:206–211 Hoflich G, Wiehe W, Hecht-Buchholz CC (1995) Rhizosphere colonization Haansuu P, Vuorela P, Haahtela K (1999) Detection of antimicrobial of different crops with growth promoting Pseudomonas and 2+ and 45Ca -transport blocking activity in Frankia culture broth Rhizobium bacteria. Microbiol Res 150:139–147 extracts. Pharm Pharmacol Lett 1:1–4 Huang XD, El-Alawi Y, Penrose DM, Glick BR, Greenberg BM Hagen G (1990) The control of gene expression by auxin. In: Davies (2004) A multiprocess phytoremediation system for removal of PJ (ed) Plant hormones and their role in plant growth and polycyclic aromatic hydrocarbons from contaminated soils. development. Kluwer, Dordrecht, pp 149–163 Environ Pollut 130:465–476 Halder AK, Chakrabarty PK (1993) Solubilization of inorganic Huang XD, El-Alawi Y, Gurska J, Glick BR, Greenberg BM (2005) A phosphate by Rhizobium. Folia Microbiol 38:325–330 multi-process phytoremediation system for decontamination of Halder AK, Mishra AK, Bhattacharya P, Chakrabarthy PK (1990) persistent total petroleum hydrocarbons (TPHs) from soils. Solubilization of rock phosphate by Rhizobium and Bradyrhizobium. Microchem J 81:139–147 J Gen Appl Microbiol 36(8):1–92 Hurek T, Reinhold-Hurek B, Van Montagu M, Kellenberger E (1994) Halder AK, Misra AK, Chakrabarty PK (1991) Solubilization of inorganic Root colonization and systemic spreading of Azoarcus sp. strain phosphates by Bradyrhizobium. Indian J Exp Biol 29:28–31 BH72 in grasses. J Bacteriol 176:1913–1923 Hardarson G (1993) Methods for enhancing symbiotic nitrogen Hynes RK, Leung GCY, Hirkala DLM, Nelson LM (2008) Isolation, fixation. Plant Soil 152:1–17 selection, and characterization of beneficial rhizobacteria from Hass D, Keel C (2003) Regulation of antibiotic production in root- pea, lentil and chickpea grown in western Canada. Can J Microb colonizing Pseudomonas sp. and relevance for biological control 54:248–258 of plant disease. Annu Rev Phytopathol 41:117–153 Idriss EE, Makarewicz O, Farouk A, Rosner K, Greiner R, Bochow H, Hayat R (2005) Sustainable legume cereal cropping system through Richter T, Borriss R (2002) Extracellular phytase activity of management of biological nitrogen fixation in Pothwar. PhD Bacillus amyloliquefaciens FZB45 contributes to its plant- Dissertation. PMAS Arid Agriculture University, Rawalpindi, growth-promoting effect. Microbiology 148:2097–2109 Pakistan Igual JM, Valverde A, Cervantes E, Velázquez E (2001) Phosphate- Hayat R, Ali S (2004) Potential of summer legumes to fix nitrogen solubilizing bacteria as inoculants for agriculture: use of updated and benefit wheat crop under rainfed condition. J Agronomy molecular techniques in their study. Agronomie 21:561–568 3:273–281. Illmer P, Schinner F (1992) Solubilization of inorganic phosphates by Hayat R, Ali S (2010) Nitrogen fixation of legumes and yield of wheat microorganisms isolated from forest soil. Soil Biol Biochem under legumes-wheat rotation in Pothwar. Pak J Bot 42(3): in press 24:389–395 Hayat R, Ali S, Siddique MT, Chatha TH (2008a) Biological nitrogen Iruthayaraj MR (1981) Let Azotobacter supply nitrogen to cotton. fixation of summer legumes and their residual effects on Intensive Agric 19-23 subsequent rainfed wheat yield. Pak J Bot 40(2):711–722 Islam N, Rao CVS, Kennedy IR (2002) Facilitating a N -fixing Hayat R, Ali S, Ijaz SS, Chatha TH, Siddique MT (2008b) Estimation of symbiosis between diazotrophs and wheat. In: Kennedy IR, N -fixation of mung bean and mash bean through xylem uriede Choudhury ATMA (eds) Biofertilisers in action. Rural Industries technique under rainfed conditions. Pak J Bot 40(2):723–734 Research and Development Corporation, Canberra, pp 84–93 Hegazi NA, Faye M, Amin G, Hamza MA, Abbas M, Youssef H, Monib Jackson MB (1991) Ethylene in root growth and development. In: M (1998) Diazotrophs assoiciated with non-legumes grown in sandy Matoo AK, Suttle JC (eds) The plant hormone ethylene. CRC soil. In: Malik KA, Mirza MS, Ladha JK (eds) Nitrogen fixation Press, Boca Raton, pp 159–181 with non-legumes. Kulwer, Dordrecht, pp 209–222 Jadhav RS, Thaker NV, Desai A (1994) Involvement of the Herman MAB, Nault BA, Smart CD (2008) Effects of plant growth siderophore of cowpea Rhizobium in the iron nutrition of the promoting rhizobacteria on bell pepper production and green peanut. World J Microbiol Biotechnol 10:360–361 peach aphid infestation in New York. Crop Prot 27:996–1002 James EK, Reis VM, Olivares FL, Baldani JI, Döbereiner J (1994) Herridge DF, Marcellos H, Felton WL, Turner GL, Peoples MB Infection of sugar cane by the nitrogen-fixing bacterium (1993) Legume N fixation an efficient source of N for cereal Acetobacter diazotrophicus. J Exp Bot 45:757–766 production, Nuclear methods in soil-plant aspects of sustainable James EK, Gyaneshwar P, Barraquio WL, Mathan N, Ladha JK agriculture (Proc. Sem. Colombo, 1993). IAEA, Vienna (2000) Endophytic diazotrophs associated with rice. In: Ladha Hesselmann RPX, Werlen C, Hahn D, van der Meer JR, Zehnder AJB JK, Reddy PM (eds) The quest for nitrogen fixation in rice. (1999) Enrichment, phylogenetic analysis and detection of a International Rice Research Institute, Los Banõs, pp 119–140 bacterium that performs enhanced biological phosphate removal Jetiyanon K, Kloepper JW (2002) Mixtures of plant growth promoting in activated sludge. Syst Appl Microbiol 22:454–465 rhizobacteria for induction of systemic resistance against multiple Hilali A, Przrost D, Broughton WJ, Antoun A (2000) Potential use of plant diseases. Biol Control 24:285–291 Rhizobium leguminosarum by trifoli as plant growth promoting Joo GJ, Kin YM, Kim JT, Rhee IK, Kim JH, Lee IJ (2005) rhizobacteria with wheat. In: Abstract of the I7th North American Gibberellins producing rhizobacteria increase endogenous conference on symbiotic nitrogen fixation. Laval University, gibberellins content and promote growth of red peppers. J Quebec, Canada, pp 23-28 Microbiol 43(6):510–515 Hilali A, Prevost D, Broughton WJ, Anloun H (2001) Effects of in- Kajar B, Jensen J (1995) The inheritance of nitrogen and phosphorous oculation avec des souches de Rhizobium leguminosarum biovar content in barley analyzed by genetic markers. Heriditas trifolii sur la croissance du ble dans deux sols du Maroc. Can J 123:109–119 Microbiol 47:590–593 Kanungo PK, Panda D, Adhya TK, Ramakrishnan B, Rao VR (1997) Hoflich G (2000) Colonization and growth promotion of non-legumes Nitrogenase activity and nitrogen fixing bacteria associated with by Rhizobium bacteria. Micobial biosystems: new prontiers. In: rhizosphere of rice cultivars. J Sci Food Agric 73:485–488 594 Ann Microbiol (2010) 60:579–598 Keating JDH, Chapmanian N, Saxena MC (1998) Effect of improved suppression of Meloidogyne incognita on tomato (Lycopersicon management of legumes in a legume-cereal rotation on field esculentum). J Nematol 34:362–369 estimates of crop nitrogen uptake and symbiotic nitrogen fixation Kokalis-Burelle N, Vavrina CS, Rosskopf EN, Shelby RA (2002b) in northern Syria. J Agric Sci 110:651–659 Field evaluation of plant growth-promoting rhizobacteria amended transplant mixes and soil solarization for tomato and Kempster VN, Scott ES, Davies KA (2002) Evidance for systematic, pepper production in Florida. Plant Soil 238:257–266 cross-resistance in white clover (Trifolium repens) and annual medic (Medicago truncatula var truncatula) induced by biological Kokalis-Burelle N, Vavrina CS, Reddy MS, Kloepper JW (2003) and chemical agents. Biocontrol Sci Technol 12(5):615–623 Amendment of muskmelon and watermelon transplant media Kennedy IR, Tchan Y (1992) Biological nitrogen fixation in no with plant growth-promoting rhizobacteria: effects on disease and leguminous field crops: recent advances. Plant Soil 141:93–118 nematode resistance. Hortic Technol 13:476–482 Kennedy IR, Islam N (2001) The current and potential contribution of Kokalis-Burelle N, Kloepper JW, Reddy MS (2006) Plant growth- asymbiotic nitrogen requirements on farms: a review. Aust J Exp promoting rhizobacteria as transplant amendments and their Agric 41:447–457 effects on indigenous rhizosphere microorganisms. Appl Soil Kennedy IR, Pereg-Gerk LL, Wood C, Deaker R, Glichrist K, Ecol 31(1–2):91–100 Katupitiya S (1997) Biological nitrogen fixation in non- Kolb W, Martin P (1985) Response of plant roots to inoculation with leguminous field crops: facilitating the evolution of an Azospirillum brasilense and to application of indoleacetic acid. effective association between Azosirillun and wheat. Plant Soil In: Klingmüller W (ed) Azospirillum III: genetics, physiology, 194:65–79 ecology. Springer, Berlin, pp 215–221 Kennedy IR, Choudhury AIMA, KecSkes ML (2004) Non-Symbiotic Kumar V, Behl RK, Narula N (2001) Establishment of phosphate bacterial diazotrophs in crop-farming systems: can their potential solubilizing strains of Azotobacter chroococcum in the rhizosphere for plant growth promotion be better exploited? Soil Boil and their effect on wheat cultivars under greenhouse conditions. Biochem 3 6(8):1229-1244 Microbiol Res 156:87–93 Kerovuo J, Lauraeus M, Nurminen P, Kalkinen N, Apajalahti J (1998) Ladha JK, Reddy PM (2003) Nitrogen fixation in rice systems: state Isolation, characterization, molecular gene cloning, and sequencing of knowledge and future prospects. Plant Soil 252:151–167 of a novel phytase from Bacillus subtilis. Appl Environ Microbiol Ladha JK, Baraquio WL, Watanabe I (1982) Immunological techniques 64:2079–2085 to identify Azospirillum associated with rice. Can J Microbiol Khalid A, Arshad M, Zahir ZA (2001) Factor affecting auxin 28:478–485 biosynthesis by wheat and rice rhizobacteria. Pak J Soil Sci Lebuhn M, Heulin T, Hartmann A (1997) Production of auxin and other 21:11–18 indolic and phenolic compounds by Paenibacillus polymyxa strains Khalid A, Arshad M, Zahir ZA (2003) Growth and yield response of isolated from different proximity to plant roots. FEMS Microbiol wheat to inoculation with auxin producing plant growth Ecol 22:325–334 promoting rhizobacteria. Pak J Bot 35:483–498 Lee S, Pierson B, Kennedy C (2002) Genetics and biochemistry of Khalid A, Arshad M, Zahir ZA (2004) Screening plant growth- nitrogen fixation and other factors beneficial to host plant growth promoting rhizobacteria for improving groth and yield of wheat. in diazotrophic endophytes. In: Vanderleyden J (ed) Proceedings J Appl Microbiol 96:473–480 of the ninth international symposium on nitrogen fixation with Khan AG (2005) Role of soil microbes in the rhizosphere of plants nonlegumes. Katholique Universiteit, Leuven, pp 41–42 growing on trace metal contaminated soils in phytoremediation. J Leelahawonge C, Nuntagij A, Teaumroong N, Boonkerd N, Pongsilp N Trace Elem Med Biol 18:355–364 (2010) Characterization of root-nodule bacteria isolated from the Kim YO, Lee JK, Kim HK, Yu JH, Oh TK (1998) Cloning of the medicinal legume Indigofera tinctoria. Ann Microbiol 60:65–74 thermo stable phytase gene (phy) from Bacillus sp. DS11 and its Lhuissier FGP, de Ruijter NCA, Sieberer BJ, Esseling JJ, Emons over expression in Escherichia coli. FEMS Microbiol Lett AMC (2001) Time course of cell biological events evoked in 162:185–191 legume root hairs by Rhizobium Nod factors: state of the art. Ann Klee HJ, Hayford MB, Kretzmer KA, Barry GF, Kishore GM (1991) Bot 87:289–302 Control of ethylene synthesis by expression of a bacterial enzyme Li J, Ovakin DH, Charles TC, Glick BR (2000) An ACC deaminase in transgenic tomato plants. Plant Cell 3:1187–1193 minus mutatnt of Entreobacter cloacae UW4 no longer promotes Kloepper JW (1993) Plant growth promoting rhizobacteria as root elongation. Curr Microbiol 41:101–105 biological control agents. In: Metting FB Jr (ed) Soil microbial Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R ecology. Dekker, New York, pp 255–274 (2003) LysM domain receptor kinase regulating rhizobial nod Kloepper JW (1994) Plant growth promoting rhizobacteria. In: Okon factor-induced infection. Science 302:630–633 Y (ed) Azospirillum/Plant associations. CRC Press, Boca Raton, Loper JE, Buyer JS (1991) Siderophores in microbial interactions on pp 137–166 plant surfaces. Mol Plant Microb Interact 4:5–13 Kloepper JW, Schroth MN (1978) Plant growth promoting rhizobacteria Lucas GJA, Probanza A, Ramos B, Colon Flores JJ, Gutierrez Mañero on radishes. Proceedings of the Fourth International Conference on FJ (2004a) Effect of plant growth promoting rhizobacteria Plant Pathogen Bacteria, vol. 2. INRA, pp 879–882 (PGPRs) on biological nitrogen fixation, nodulation and growth Kloepper JW, Beauchamp CJ (1992) A review of issues related to of Lupinus albus I. cv. Multolupa. Eng Life Sci 7:1–77 measuring colonization of plant roots by bacteria. Can J Microbiol Lucas GJA, Probanza A, Ramos B, Palomino MR, Gutierrez Mañero 38:1219–1232 FJ (2004b) Effect of inoculation of Bacillus licheniformis on Kloepper JW, Lifshitz R, Zablotowicz RM (1989) Free-living bacterial tomato and pepper. Agronomie 24:169–176 inocula for enhancing crop productivity. Trends Biotechnol 7:39–43 Lupwayi NZ, Rice WA, Clayton GW (2000) Endophytic Rhizobia in Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance barley and canola in rotation with field peas. In: Book of and promotion of plant growth by Bacillus spp. Phytopathology abstracts, 17th North American conference on symbiotic nitrogen 94(11):1259–1266 fixation, 23-28 July 2000, 80. University of Laval, Quebec, Kokalis-Burelle N (2003) Effects of transplant type and soil fumigant on Canada, p 51 growth and yield of strawberry in Florida. Plant Soil 256:273–280 Lynch JM (1983) Soil biotechnology. Blackwell, Oxford Kokalis-Burelle N, Martinez-Ochoa N, Rodríguez-Kábana R, Kloepper Lynch JM (1990) Beneficial interactions between miroorganisms and JW (2002a) Development of multi-component transplant mixes for roots. Biotechnol Adv 8:335–346 Ann Microbiol (2010) 60:579–598 595 Malik KA, Mirza MS, Hassan U, Mehnaz S, Rasul G, Haurat J, Bauy Narasimhan K, Basheer C, Bajic VB, Swarup S (2003) Enhancement of R, Normanel P (2002) The role of plant associated beneficial plant-microbe interactions using a rhizosphere metabolomics-driven bacteria in rice-wheat Cropping System. In: Kennedy IR, approach and its application in the removal of polychlorinated Chaudhry ATMA (eds) Biofertilisers in action. Rural industries biphenyls. Plant Physiol 132:146–153 research and development Corporation, Canberra, pp 73–83 Nautiyal CS, Bhadauria S, Kumar P, Lal H, Mondal R, Verma D Mantelin S, Touraine B (2004) Plant growth-promoting bacteria and (2000) Stress induced phosphate solubilization in bacteria nitrate availability: impacts on root development and nitrate isolated from alkaline soils. FEMS Microbiol Lett 182:291–296 uptake. J Exp Bot 55:27–34 Nieto KF, Frankenberger WT Jr (1990a) Influence of adenine, Martinez-Romero E, Gutierrez-Zamora ML, Estrada P, Caballero- isopentyl alcohol and Azotobacter chroococcum on the growth Mellado J, Hernandez-Lucas I (2000) Natural endophytic associa- of Raphanus sativus. Plant Soil 127:147–156 tion between Rhizobium Etli and maize. In: Book of abstracts, 17th Nieto KF, Frankenberger WT Jr (1990b) Microbial production of North American conference on symbiotic nitrogen fixation, 23-28 cytokinins. In: Bollag JM, Stotzky G (eds) Soil biochem, vol 6. July 2000. University of Laval, Quebec, Canada, p 51 Dekker, New York, pp 191–248 Martinez-Toledo MV, Rodelas B, Salmeron V, Pozo C, Gonzalez- Nieto KF, Frankenberger WT Jr (1991) Influence of adenine, isopentyl Lopez J (1996) Production of pantothenic acid and thiamine by alcohol and Azotobacter chroococcum on the vegetative growth Azotobacter vinelandii in a chemically defined medium and a of Zea mays. Plant Soil 135:213–221 dialysed soil medium. Biol Fertil Soils 22:131–135 Noling JW, Gilreath JP (2001) Methyl bromide, progress and Matiru VN, Dakora FD (2004) Potential use of rhizobial bacteria as problems: identifying alternatives to methyl bromide, vol. II. promoters of plant growth for increased yield in landraces of Citrus and Veg. Mag., IFAS, University of Florida African cereal crops. Afr J Biotechnol 3(1):1–7 O´Sullivan DJ, O´Gara F (1992) Traits of fluorescent Pseudomonas McGrathJW, Wisdom GB,McMullanG,Lrakin MJ, QuinnJP spp. involved in suppression of plant root pathogens. Microbiol (1995) The purification and properties of phosphonoacetate Rev 56:662–676 hydrolase, a novel carbon-phosphorus bond-cleaving enzyme Ohr HD, Sims JJ, Grech NM, Becker JO, McGiffen ME Jr (1996) from Pseudomonas fluorescens 23F. Eur J Biochem 234:225– Methyl iodide, an ozone-safe alternative to methyl bromide as a soil fumigant. Plant Dis 80:27–32 McGrath JW, Hammerschmidt F, Quinn JP (1998) Biodegradation of Ohtake H, Wu H, Imazu K, Ambe Y, Kato J, Kuroda A (1996) phosphonomycin by Rhizobium huakuii PMY1. Appl Environ Bacterial phosphonate degradation, phosphite oxidation and Microbiol 64:356–358 polyphosphate accumulation. Res Conserv Recycl 18:125–134 Mclnroy JA, Kloepper JW (1995) Survey of indigenous endophytes Okon Y, Labandera-Gonzalez CA (1994) Agronomic applications of from cotton and sweet corn. Plant Soil 173:337–342 Azospirillum: an evaluation of 20 years world-wide field Meyer SLF, Massoud SI, Chitwood DJ, Roberts DP (2000) Evaluation inoculation. Soil Biol Biochem 26:1591–1601 of Trichoderma virens and Burkholderia cepacia for antagonistic Okon Y, Itzigsohn R (1995) The development of Azospirillum as a activity against root-knot nematode, Meloidogyne incognita. commercial innoculant for improving crop yields. Biotechnol Nematology 2:871–879 Adv 13(3):415–424 Middledrop PJM, Briglia M, Salkinoja-Salonen M (1990) Biodeg- Pal KK, Tilak KVBR, Saxena AK, Dey R, Singh CS (2001) radation of pentachlorophenol in natural polluted soil by Suppression of maize root diseases caused by Macrophomina inoculated Rhodococcus chlorophenolicus.MicrobEcol phaseolina, Fusarium moniliforme and Fusarium germinearum 20:123–139 by plant growth promoting rhizobacteria. Microbiol Res Miller RM, Jastrow JD (2000) Mycorrhizal fungi influence soil 156:209–223 structure. In: Kapulnik Y, David DD, David DD Jr (eds) Pandey A, Kumar S (1989) Potential of Azotobacters and Azospirilla Arbuscular mycorrhizas: physiology and function. Springer, as biofertilizers for upland agriculture: a review. J Sci Ind Res Berlin 48:134–144 Milton HSJ (2007) Beneficial bacteria and bioremediation. Water Air Panwar JDS, Singh O (2000) Response of Azospirillum and Bacillus Soil Pollut 184:1–3 on growth and yield of wheat under field conditions. Indian J Mirza MS, Rasul G, Mehnaz S, Ladha JK, So RB, Ali S, Malik KA Plant Physiol 5:108–110 (2000) Beneficial effects of inoculated nitrogen-fixing bacteria on Park KS, Kloepper JW (2000) Activation of PR-1a promoter by rice. In: Ladha JK, Reddy PM (eds) The quest for nitrogen rhizobacteria which induces systemic resistance in tobacco fixation in rice. International Rice Research Institute, Los Banõs, against Pseudomonas syringae pv. Tabaco Biol Cont 18:2–9 pp 191–204 Patil PL, Patil SP (1984) Uptake of nitrogen by cotton inoculated with Muratova A Yu, Turkovskaya OV, Antonyuk LP, Makarov OE, Azotobacter. J Maharashtra Agric Uni 9(17):1–172 Pozdnyakova LI, Ignatov VV (2005) Oil-oxidizing potential of Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic associative rhizobacteria of the genus Azospirillum. Microbiology acid. Can J Microbiol 42:207–220 74:210–215 Patten CL, Glick BR (2002) Role of Pseudomonas putida indole-acetic Murphy JF, Zender GW, Schuster DJ, Sikora EJ, Polston JE, Kloepper acid in development of the host plant root system. Appl Environ JW (2000) Plant growth promoting rhizobacterial mediated Microbiol 68:3795–3801 protection in tomato against tomato mottle virus. Plant Dis Paynel F, Murray PJ, Cliquet B (2001) Root exudates: a pathway for 84:779–784 short-term N transfer from clover and ryegrass. Plant Soil Murray JD, Bogumil JK, Shusei SH, Satoshi T, Lisa A, Krzysztof S 229:235–243 (2007) A cytokinin perception mutant colonized by Rhizobium in Peix A, Rivas-Boyero AA, Mateos PF, Rodriguez-Barrueco C, the absence of nodule organogenesis. Science 315(5808):101–104 Martínez-Molina E, Velazquez E (2001) Growth promotion of Muthukumarasamy R, Revathi G, Lakshminarasimhan C (1999) chickpea and barley by a phosphate solubilizing strain of Diazotrophic associations in sugar cane cultivation in South Mesorhizobium mediterraneum under growth. Soil Biol Biochem India. Trop Agric 76:171–178 33:103–110 Nakata PA (2002) The generation of a transposon-mutagenized Pereira JAR, Cavalcante VA, Baldani JI, Döbereiner J (1988) Field Burkholderia glumae library to isolate novel mutants. Plant Sci inoculation of sorghum and rice with Azospirillum sp and 162:267–271 Herbaspirillum seropedicae. Plant Soil 110:269–274 596 Ann Microbiol (2010) 60:579–598 Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the Roesti D, Guar R, Johri BN, Imfeld G, Sharma S, Kawaljeet K, Aragno M underground: molecular plant-rhizobacteria interactions. Plant (2006) Plant growth stage, fertilizer management and bio- Cell Environ 26:189–199 inoculation of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria affect the rhizobacterial community Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, structure in rain-fed wheat field. Soil Biol Biochem 38:1111–1120 Machado De Oliveira R, Leid M, McBurney MW, Guarente L (2004) Sirt1 promotes fat mobilization in white adipocytes by Roper MM, Ladha JK (1995) Biological N -fixation by heterotrophic repressing PPAR-gamma. Nature 429(77):1–776 and phototrophic bacteria in association with straw. Plant Soil Plessner O, Klapach T, Guerinot ML (1993) Siderophore utilization by 174:211–224 Bradyrhizobium japonicum. Appl Environ Microbiol 59:1688– Rossolini GM, Shipa S, Riccio ML, Berlutti F, Macaskie LE, Thaller 1690 MC (1998) Bacterial non-specific acid phosphatases: physiology, evolution, and use as tools in microbial biotechnology. Cell Mol Primrose SB (1979) Ethylene and agriculture: the role of the microbe. Life Sci 54:833–850 J Appl Bacteriol 46:1–25 Raj SN, Deepak SA, Basavaraju P, Shetty HS, Reddy MS, Kloepper JW Russo A, Vettori L, Felici C, Fiaschi G, Morini S, Toffanin A (2008) Enhanced cropropagation response and biocontrol effect of (2003) Comparative performance of formulations of plant growth Azospirillum brasilense Sp245 on Prunus cerasifera L. clone promoting rhizobacteria in growth promotion and suppression of Mr.S 2/5 plants. J Biotechnol 134(3–4):312–319 downy mildew in pearl millet. Crop Prot 22:579–588 Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW Rao DLN (2001) BNF research progress 1996-2000: all India (2004) Bacterial volatiles induce systemic resistance in Arabi- coordinated research project on biological nitrogen fixation. dopsis. Plant Physiol 134:1017–1026 IISS, Bhopal Ryu CM, Kim J, Choi O, Kim SH, Park CS (2006) Improvement of Reid M (1987) Ethylene in plant growth, development and biological control capacity of Paenibacillus polymyxa E681 by senescence. In: Davies PJ (ed) Plant hormones and their role seed pelleting on sesame. Biol Control 39:282–289 in plant growth and development. Martinus Nijhoff, Boston, Şahin F, Çakmakçi R, Kantar F (2004) Sugar beet and barley yields in pp 257–279 relation to inoculation with N -fixing and phosphate solubilizing Reilly TJ, Baron GS, Nano F, Kuhlenschmidt MS (1996) bacteria. Plant Soil 265:123–129 Characterization and sequencing of a respiratory burst Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of inhibiting acid phosphatase from Francisella tularensis.JBiol Chem 271:10973–10983 plant growth promoting rhizobacteria (PGPR) containing ACC Reinhold-Hurek B, Hurek T, Gillis M, Hoste B, Vancanneyt M, deaminase in stress agriculture. J Ind Microbiol Biotechnol Kersters K, DeLey J (1993) Azoarcus gen. nov., nitrogen fixing 34:635–648 proteobacteria associated with roots of Kallar grass (Leptochloa Saleh S, Huang XD, Greenberg BM, Glick BR (2004) Phytoremedia- fusca (L.) Kunth) and description of two species, Azoarcus tion of persistent organic contaminants in the environment. In: indigens sp. nov. and Azoarcus communis sp. nov. Int J Syst Singh A, Ward O (eds) Soil biology, vol. 1. Applied bioreme- Bacteriol 43:574–584 diation and phytoremediation. Springer, Berlin, pp 115–134 Reinhold-Hurek B, Egener T, Hurek T, Martin D, Sarkar A, Zhang L, Saravanakumar D, Lavanya N, Muthumeena B, Raguchander T, Miche L (2002) Regulation of nitrogen fixation and assimilation Suresh S, Samiyappan R (2008) Pseudomonas fluorescens of Azoarcus sp. BH72 new approaches to study biodiversity of enhances resistance and natural enemy population in rice plants grass endophytes. In: Vanderleyden J (ed) Proceedings of the against leaf folder pest. J Appl Entomol 132(6):469–479 nineth international symposium on nitrogen fixation with non- Sasikala C, Ramana CV (1995) Biotechnological potentials of legumes. Katholique Universideit Leuven, Belgium, p 48 anoxygenic phototrophic bacteria. I. Production of single-cell Reis VM, Baldani JI, Baldani VLD, Döberener J (2000) Biological protein, vitamins, ubiquinones, hormones, and enzymes and use in waste treatment. Adv Appl Microbiol 41:173–226 dinitrogen fixation in the graminae and palm trees. Crit Rev Plant Saubidet MI, Fatta N, Barneix AJ (2000) The effects of inoculation Sci 19:227–247 with Azospirillum brasilense on growth and nitrogen utilization Revillas JJ, Rodelas B, Pozo C, Martinez-Toledo MV, Gonzalez LJ by wheat plants. Plant Soil 245(2):15–222 (2000) Production of B-group vitamins by two Azotobacter Schippers B, Bakker AW, Baker PAHM (1987) Interactions of strains with phenolic compounds as sole carbon source under deleterious and beneficial rhizosphere microorganisms and the diazotrophic and adiazotrophic conditions. J Appl Microbiol effect of cropping practices. Annu Rev Phytopathol 25:339–358 89:486–493 Schippers B, Scheffer RJ, Lugtenberg JJ, Weisbek PJ (1995) Richardson AE (2001) Prospects for using soil microorganisms to Biocoating of seed with plant growth promoting rhizobacteria improve the acquisition of phosphorus by plants. Aust J Plant to improve plant establishment. Outlook Agric 24:179–185 Physiol 28:897–906 Schloter M, Wiehe W, Assmus B, Steindl H, Becke H, Hoflich G, Richardson AE, Hadobas PA (1997) Soil isolates of Pseudomonas Hartman A (1997) Root colonization of different plants by plant spp. that utilize inositol phosphates. Can J Microbiol 43(509– growth-promoting Rhizobium leguminosarum bv trifolii R39 5):16 Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their studied with monospecific polyclonal antisera. Appl Environ role in plant growth promotion. Biotechnol Adv 17:319–339 Microbiol 63:2038–2046 Rodríguez H, Han Y, Lei XG (1999) Cloning, sequencing and Séguin A, Lalonde M (1989) Detection of pectolytic activity and pel expression of an Escherichia. coli acid phopshatase/phytase gene homologous sequences in Frankia. Plant Soil 118:221–229 (app A2) isolated from pig colon. Biochem Biophys Res Serrano A, Mateos MI, Losada M (1993) Differential regulation by Commun 257:117–123 trophic conditions of phosphorylating and nonphosphorylating Rodríguez H, Rossolini GM, Gonzalez T, Jiping L, Glick BR (2000) NADP(+)-dependent glyceraldehyde-3-phosphate dehydro- Isolation of a gene from Burkholderia cepacia IS-16 encoding a genases in Chlorella fusca. Biochem Biophys Res Commun protein that facilitates phosphatase activity. Curr Microbiol 193:1348–1356 40:362–366 Shah Z, Shah SH, Peoples MB, Schwenke GD, Hrridge DF (2003) Rodríguez H, Fraga R, Gonzalez T, Bashan T (2006) Genetics of Crop residue and fiertilizer N effects on nitrogen fixation and phosphate solubilization and its potential applications for improving yields of legume-cereal rotations and soil organic fetility. Field plant growth-promoting bacteria. Plant Soil 287:15–21 Crops Res 83:1–11 Ann Microbiol (2010) 60:579–598 597 Shaharoona B, Arshad M, Zahir ZA (2006a) Effect of plant growth Thaller MC, Berlutti F, Schippa S, Lombardi G, Rossolini GM promoting rhizobacteria containing ACC-deaminase on maize (Zea (1994) Characterization and sequence of PhoC, the principal mays L.) growth under axenic conditions and on nodulation in phosphate-irrepressible acid phosphatase of Morganella mung bean (Vigna radiata L.). Lett Appl Microbiol 42:155–159 morganii. Microbiology 140:1341–1350 Shaharoona B, Arshad M, Zahir ZA, Khalid A (2006b) Performance Thaller MC, Berlutti F, Schippa S, Iori P, Passariello C, Rossolini GM of Pseudomonas spp. containing ACC-deaminase for improving (1995a) Heterogeneous patterns of acid phosphatases containing growth and yield of maize (Zea mays L.) in the presence of low-molecular-mass Polipeptides in members of the family nitrogenous fertilizer. Soil Biol Biochem 38:2971–2975 Enterobacteriaceae. Int J Syst Bacteriol 4:255–261 Shankariah C, Hunsigi G (2001) Field responses of sugarcane to Thaller MC, Lombardi G, Berlutti F, Schippa S, Rossolini GM (1995b) associative N fixers and P solubilishers. In: Hogarth DM (ed) Cloning and characterization of the NapA acid phosphatase/ Proceedings of the 24th international society of sugarcane phosphotransferase of Morganella morganii: identification of a Technologists Congress, 17-21 September 2001. The Australian new family of bacterial acid phosphatase encoding genes. Society of Sugercane Technologists, Brisbane, pp 40–45 Microbiology 140:147–151 Shenoy VV, Kalagudi GM (2005) Enhancing plant phosphorus use Tien TM, Diem HG, Gaskins MH, Hubbell DH (1981) Polygaracturonic efficiency for sustainable cropping. Biotechnol adv 23:501–513 acid transeliminase production by Azospirillum species. Can J Shiferaw B, Bantilan MCS, Serraj R (2004) Harnessing the potential Microbiol 27:426–431 of BNF for poor farmers: technological policy and institutional Tisdale SL, Nelson WL, Beaton JD (1990) Soil fertility and fertilizers, constraints and research need. In: Serraj R (ed) Symbiotic 4th edn. Macmillan, New York nitrogen fixation; prospects for enhanced application in tropical Tran Vân V, Berge O, Ke SN, Balandreau J, Heulin T (2000) Repeated agriculture. Oxford & IBH, New Delhi, p 3 beneficial effects of rice inoculation with a strain of Burkholderia Shoebitz M, Ribaudo CM, Pardo MA, Cantore ML, Ciampi L, Curá vietnamiensis on early and late yield components in low fertility JA (2009) Plant growth promoting properties of a strain of sulphate acid soils of Vietnam. Plant Soil 218:273–284 Enterobacter ludwigii isolated from Lolium perenne rhizosphere. Tye AJ, Siu FK, Leung TY, Lim BL (2002) Molecular cloning and the Soil Biol Biochem 41(9):1768–1774 biochemical characterization of two novel phytases from Bacillus Siddiqui IA, Ehteshamul-Haque S, Shaukat SS (2001) Use of subtilis 168 and Bacillus licheniformis. Appl Microbiol Biotechnol rhizobacteria in the control of root rot-root knot disease complex 59:190–197 of mung bean. J Phytopathol 149:337–346 Umali-Garcia M, Hubbell DH, Gaskins MH, Dazzo FB (1980) Sierra S, Rodelas B, Martinez-Toledo MV, Pozo C, Gonzalez-Lopez J Association of Azospirillum with grass roots. Appl Environ (1999) Production of B-group vitamins by two Rhizobium strains Microbiol 39(1):219–226 in chemically defined media. J Appl Microbiol 86:851–858 Valverde F, Losada M, Serrano A (1999) Engineering a central Skrary FA, Cameron DC (1998) Purification and characterization of a metabolic pathway: glycolysis with no net phosphorylation in an Bacillus licheniformis phosphatase specific for D-alpha- Escherichia coli gap mutant complemented with a plant Gap N glycerphosphate. Arch Biochem Biophys 349:27–35 gene. FEBS Lett 449:153–158 Snapp SS, Aggarwal VD, Chirwa RM (1998) Note on phosphorus and van Loon LC, Bakker P, Pieterse CMJ (1998) Systemic resistance induced genotype enhancement of biological nitrogen fixation and productiv- by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483 ity of maize/bean intercrops in Malawi. Field Crops Res 58:205–212 Van Rhijn P, Fujishige NA, Lim PO, Hirsch AM (2001) Sugar-binding Soliman S, Seeda MA, Aly SSM, Gadalla AM (1995) Nitrogen activity of pea lectin enhances heterologous infection of fixation by wheat plants as affected by nitrogen fertilizer levels transgenic alfalfa plants by Rhizobium leguminosarum bivor and nonsymbiotic bacteria. Egypt J Soil Sci 35:401–413 viciae. Plant Physiol 126:133–144 Spencer D, James EK, Ellis GJ, Shaw JE, Sprent JI (1994) Interactions Van Veen JA, van Overbeek LS, van Elsas JD (1997) Fate and activity between Rhizobia and potato tissue. J Exp Bot 45:1475–1482 of microorganisms introduced into soil. Microbiol Mol Biol Rev Stajner D, Gasaić O, Matković B, Varga SZI (1995) Metolachlor 61:121–135 effect on antioxidants enzyme activities and pigments content in Vandamme P, Goris J, Chen WM, de Vos P, Willems A (2002) seeds and young leaves of wheat (Triticum aestivum L.). Agr Burkholderia tuberum sp. nov and Burkholderia phymatum sp. Med 125:267–273 nov., nodulate the roots of tropical legumes. Syst Appl Microbiol Stajner D, Kevreaan S, Gasaić O, Mimica-Dudić N, Zongli H (1997) 25:507–512 Nitrogen and Azotobacter chroococcum enhance oxidative stress Venkateswarlu B, Hari K, Katyl JC (1997) Influence of soil and crop tolerance in sugar beet. Biol Plant 39:441–445 factors on the native rhizobia populations in soils under dry land Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living farming. Appl Soil Ecol 7:1–10 nitrogen-fixing bacterium closely associated with grasses: genetic, Vestberg M, Kukkonen S, Saari K, Parikka P, Huttunen J, Tainino L, biochemical and ecological aspects. FEMS Microbiol Rev Devos N, Weekers F, Kevers C, Thonart P, Lemoine MC, Cordier C, 24:487–506 Alabouvette C, Gianinazzi S (2004) Microbial inoculation for Stout MJ, Zehnder GW, Baur ME (2002) Potential for the use of improving the growth and health of micropropagated strawberry. elicitors of plant defence in arthropode management programs. Appl Soil Ecol 27:243–258 Arch Insect Biochem Physiol 51(4):222–235 Vivas A, Barea JM, Azcón R (2005) Brevibacillus brevis isolated from Sturz AV, Christie BR, Novak J (2000) Bacterial endophytes: potential cadmium- or zinc-contaminated soils improves in vitro spore role in developing sustainable system of crop production. Crit germination and growth of Glomus mosseae under high Cd or Zn Rev Plant Sci 19:1–30 Concentrations. Microb Ecol 49:416–442 Sutton JC, Peng G (1993) Biocontrol of Botrytis cinerea in strawberry Wachowska U, Majchrzak B, Borawska M, Karpinska Z (2004) leaves. Phytopathology 83:615–621 Biological control of winter wheat pathogens by bacteria. Acta Terouchi N, Syono K (1990) Rhizobium attachment and curling in fytotech zootech, Vol. 7, 2004, Special Number, Proceedings of asparagus, rice, and oat plants. Plant Cell Physiol 31:119–127 the XVI. Slovak and Czech Plant Protection Conference Thakuria D, Taleekdar NC, Goswami C, Hazarika S, Boro RC, Khan organized at Slovak Agricultural University in Nitra, Slovakia MR (2004) Characterization and screening of bacteria from Walsh UF, Morrissey JP, O’Gara F (2001) Pseudomonas for biocontrol rhizosphere of rice grown in acidic soils of Assam. Curr Sci 86 of phytopathogens: from functional genomics to commercial (7):978–985 exploitation. Curr Opin Biotechnol 12:289–295 598 Ann Microbiol (2010) 60:579–598 Webster G, Gough C, Vasse J, Batchelor CA, O’Callaghan KJ, nodulation of lentil (Lens culinaris Medic) seedlings under Kothari SL, Davey MR, Denarie J, Cocking EC (1997) axenic conditions. Soil Environ 26(1):81–91 Interactions of Rhizobia with rice and wheat. Plant Soil Zahir AZ, Arshad M, Frankenberger WT Jr (2004) Plant growth 194:115–122 promoting rhizobacteria: application and perspectives in Agriculture. Adv Agron 81:97–168 Wiehe W, Holfich G (1995) Survival of plant growth promoting Zahir ZA, Abbas SA, Khalid M, Arshad M (2000) Substrate rhizosphere bacteria in rhizosphere of different crops and dependent microbially derived plant hormones for improving migration to non-inoculated plants under field conditions in growth of maize seedlings. Pak J Biol Sci 3:289–291 north-east Germany. Microbiol Res 150:201–206 Zaidi S, Usmani S, Singh BR, Musarrat J (2008) Significance of Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation Bacillus subtilis strains SJ-101 as a bioinoculant for concurrent in higher plants. Annu Rev Plant Physiol 35:155–189 plant growth promotion and nickel accumulation in Brassica Yanni YG, El-Fattah FKA (1999) Towards integrated biofertiliza- Juncea. Chemosphere 64:991–997 tion management with free living and associative dinitrogen fixers for enhancing rice performance in the Nile delta. Zavalin AA, Kandaurova TM, Vinogradova LV (1998) Influence of Symbiosis 27:319–331 nitrogen fixing microorganisms on the nutrition and productivity Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip- of spring wheat, and on the characteristics of photosynthesis of Hollingsworth S, Orgambide G, de Bruijn F, Stoltzfus J, Buckley different varieties of spring wheat. In: Elmerich C, Kondorosi A, D, Schmidt TM, Mateos PF, Ladha JK, Dazzo FB (1997) Natural Newton WE (eds) Biological nitrogen fixation for the 21st endophytic association between Rhizobium leguminosarum bv. century. Kluwer, Dordrecht, pp 413–414 trifolii and rice roots and assessment of its potential to promote Zhang S, Moyne AL, Reddy MS, Kloepp JW (2002) The role of rice growth. Plant Soil 194:99–114 salicylic acid in induced systemic resistance elicited by plant Yanni YG, Rizk RY, Abd El-Fattah FK, Squartini A, Corich V, growth-promoting rhizobacteria against blue mold of tobacco. Giacomini A, de Bruijn F, Rademaker J, Maya-Flores J, Biol Control 25:288–296 Ostrom P, Vega-Hernandez M, Hollingsworth RI, Martinez- Zhang H, Sekiguchi Y, Hanada S, Hugenholtz P, Kim H, Kamagata Y, Molina E, Ninke K, Philip-Hollingsworth S, Mateos PF, Nakamura K (2003) Gemmatimonas aurantiaca gen. nov., sp. nov., Velasquez E, Triplett E, Umali-Garcia M, Anarna JA, Rolfe a Gram-negative, aerobic, polyphosphate accumulating micro- BG, Ladha JK, Hill J, Mujoo R, Ng PK, Dazzo FB (2001) organism, the first cultured representative of the new bacterial The beneficial plant growth-promoting association of Rhizo- phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol 53:1155–1163 bium leguminosarum bv. trifolii with rice roots. Aust J Plant Zhuang XL, Chen J, Shim H, Bai Z (2007) New advances in plant Physiol 28:845–870 growth-promoting rhizobacteria for bioremediation. Environ Int Zafar-ul-Hye M, Zahir ZA, Shahzad SM, Irshad U, Arshad M (2007) 33:406–413 Isolation and screening of Rhizobia for improving growth and http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Annals of Microbiology Springer Journals

Soil beneficial bacteria and their role in plant growth promotion: a review

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Ann Microbiol (2010) 60:579–598 DOI 10.1007/s13213-010-0117-1 REVIEW ARTICLE Soil beneficial bacteria and their role in plant growth promotion: a review Rifat Hayat & Safdar Ali & Ummay Amara & Rabia Khalid & Iftikhar Ahmed Received: 23 February 2010 /Accepted: 29 July 2010 /Published online: 28 August 2010 Springer-Verlag and the University of Milan 2010 Abstract Soil bacteria are very important in biogeochemical includes the prevention of the deleterious effects of cycles and have been used for crop production for decades. phytopathogenic organisms. This can be achieved by the Plant–bacterial interactions in the rhizosphere are the deter- production of siderophores, i.e. small metal-binding mole- minants of plant health and soil fertility. Free-living soil cules. Biological control of soil-borne plant pathogens and bacteria beneficial to plant growth, usually referred to as plant the synthesis of antibiotics have also been reported in several growth promoting rhizobacteria (PGPR), are capable of bacterial species. Another mechanism by which PGPR can promoting plant growth by colonizing the plant root. PGPR inhibit phytopathogens is the production of hydrogen are also termed plant health promoting rhizobacteria (PHPR) cyanide (HCN) and/or fungal cell wall degrading enzymes, or nodule promoting rhizobacteria (NPR). These are associ- e.g., chitinase and ß-1,3-glucanase. Direct plant growth ated with the rhizosphere, which is an important soil promotion includes symbiotic and non-symbiotic PGPR ecological environment for plant–microbe interactions. Sym- which function through production of plant hormones such biotic nitrogen-fixing bacteria include the cyanobacteria of the as auxins, cytokinins, gibberellins, ethylene and abscisic genera Rhizobium, Bradyrhizobium, Azorhizobium, Allorhi- acid. Production of indole-3-ethanol or indole-3-acetic acid zobium, Sinorhizobium and Mesorhizobium. Free-living (IAA), the compounds belonging to auxins, have been nitrogen-fixing bacteria or associative nitrogen fixers, for reported for several bacterial genera. Some PGPR function example bacteria belonging to the species Azospirillum, as a sink for 1-aminocyclopropane-1-carboxylate (ACC), the Enterobacter, Klebsiella and Pseudomonas,havebeen immediate precursor of ethylene in higher plants, by shown to attach to the root and efficiently colonize root hydrolyzing it into α-ketobutyrate and ammonia, and in this surfaces. PGPR have the potential to contribute to sustain- way promote root growth by lowering indigenous ethylene able plant growth promotion. Generally, PGPR function in levels in the micro-rhizo environment. PGPR also help in three different ways: synthesizing particular compounds for solubilization of mineral phosphates and other nutrients, the plants, facilitating the uptake of certain nutrients from the enhance resistance to stress, stabilize soil aggregates, and soil, and lessening or preventing the plants from diseases. improve soil structure and organic matter content. PGPR Plant growth promotion and development can be facilitated retain more soil organic N, and other nutrients in the plant– both directly and indirectly. Indirect plant growth promotion soil system, thus reducing the need for fertilizer N and P and enhancing release of the nutrients. : : : R. Hayat (*) S. Ali U. Amara R. Khalid Department of Soil Science & SWC, . . . Keywords PGPR Symbiotic Non-symbiotic PMAS Arid Agriculture University, . . P-solubilization Phytohormones Biocontrol Rawalpindi 46300, Pakistan e-mail: hayat@uaar.edu.pk I. Ahmed Introduction Plant Biotechnology Program, National Agricultural Research Centre, Soil bacteria have been used in crop production for Park Road, decades. The main functions of these bacteria (Davison Islamabad, Pakistan 580 Ann Microbiol (2010) 60:579–598 1988) are (1) to supply nutrients to crops; (2) to stimulate fixing bacteria such as Azotobacter, Azospirillum, Bacillus, plant growth, e.g., through the production of plant and Klebsiella sp. are also used to inoculate a large area of hormones; (3) to control or inhibit the activity of plant arable land in the world with the aim of enhancing plant pathogens; (4) to improve soil structure; and (5) bioaccu- productivity (Lynch 1983). In addition, phosphate- mulation or microbial leaching of inorganics (Brierley solubilizing bacteria such as species of Bacillus and 1985; Ehrlich 1990). More recently, bacteria have also Paenibacillus (formerly Bacillus) have been applied to been used in soil for the mineralization of organic soils to specifically enhance the phosphorus status of plants pollutants, i.e. bioremediation of polluted soils (Middledrop (Brown 1974). et al. 1990; Burd et al. 2000; Zhuang et al 2007; Zaidi et al. PGPR have the potential to contribute in the develop- 2008). In the era of sustainable crop production, the plant– ment of sustainable agricultural systems (Schippers et al. microbe interactions in the rhizosphere play a pivotal role 1995). Generally, PGPR function in three different ways in transformation, mobilization, solubilization, etc. of (Glick 1995, 2001): synthesizing particular compounds for nutrients from a limited nutrient pool, and subsequently the plants (Dobbelaere et al. 2003; Zahir et al. 2004), uptake of essential nutrients by plants to realize their full facilitating the uptake of certain nutrients from the soil genetic potential. At present, the use of biological (Lucas et al. 2004a, b; Çakmakçi et al. 2006), and lessening approaches is becoming more popular as an additive to or preventing the plants from diseases (Guo et al. 2004; chemical fertilizers for improving crop yield in an integrat- Jetiyanon and Kloepper 2002; Raj et al. 2003; Saravana- ed plant nutrient management system. In this regard, the use kumar et al. 2008). The mechanisms of PGPR-mediated of PGPR has found a potential role in developing enhancement of plant growth and yield of many crops are sustainable systems in crop production (Sturz et al. 2000; not yet fully understood (Dey et al. 2004). However, the Shoebitz et al. 2009). A variety of symbiotic (Rhizobium possible expalination include (1) the ability to produce a sp.) and non-symbiotic bacteria (Azotobacter, Azospirillum, vital enzyme, 1-aminocyclopropane-1-carboxylate (ACC) Bacillus, and Klebsiella sp., etc.) are now being used deaminase to reduce the level of ethylene in the root of worldwide with the aim of enhancing plant productivity developing plants thereby increasing the root length and (Burd et al. 2000; Cocking 2003). growth (Li et al. 2000; Penrose and Glick 2001); (2) the Free-living soil bacteria beneficial to plant growth are ability to produce hormones like auxin, i.e indole acetic usually referred to as plant growth promoting rhizobacteria acid (IAA) (Patten and Glick 2002), abscisic acid (ABA) (PGPR), capable of promoting plant growth by colonizing (Dangar and Basu 1987; Dobbelaere et al. 2003), gibber- the plant root (Kloepper and Schroth 1978; Kloepper et al. ellic acid (GA) and cytokinins (Dey et al. 2004); (3) a 1989; Cleyet-Marcel et al. 2001). PGPR are also termed as symbiotic nitrogen fixation (Kennedy et al. 1997, 2004); (4) plant health promoting rhizobacteria (PHPR) or nodule antagonism against phytophatogenic bacteria by producing promoting rhizobacteria (NPR) and are associated with the siderophores, ß-1, 3-glucanase, chitinases, antibiotic, fluo- rhizosphere which is an important soil ecological environ- rescent pigment and cyanide (Cattelan et al. 1999; Pal et al. ment for plant–microbe interactions (Burr and Caesar 2001; Glick and Pasternak 2003); (5) solubilization and 1984). According to their relationship with the plants, mineralization of nutrients, particularly mineral phosphates PGPR can be divided into two groups: symbiotic bacteria (de Freitas et al. 1997; Richardson 2001; Banerjee and and free-living rhizobacteria (Khan 2005). PGPR can also Yasmin 2002); (6) enhanced resistance to drought (Alvarez be divided into two groups according to their residing sites: et al. 1996), salinity, waterlogging (Saleem et al. 2007) and iPGPR (i.e., symbiotic bacteria), which live inside the plant oxidative stress (Stajner et al. 1995, 1997); and (7) cells, produce nodules, and are localized inside the production of water-soluble B group vitamins niacin, pan- specialized structures; and ePGPR (i.e., free-living rhizo- tothenic acid, thiamine, riboflavine and biotin (Martinez- bacteria), which live outside the plant cells and do not Toledo et al. 1996;Sierra et al. 1999; Revillas et al. 2000). produce nodules, but still prompt plant growth (Gray and The application of PGPR has also been extended to Smith 2005). The best-known iPGPR are Rhizobia, which remediate contaminated soils in association with plants produce nodules in leguminous plants. A variety of bacteria (Zhuang et al. 2007). Thus, it is an important need to have been used as soil inoculants intended to improve the enhance the efficiency of meager amounts of external inputs supply of nutrients to crop plants. Species of Rhizobium by employing the best combinations of beneficial bacteria in (Rhizobium, Mesorhizobium, Bradyrhizobium, Azorhi- sustainable agriculture production systems. This review zobium, Allorhizobium and Sinorhizobium) have been covers the perspective of soil-beneficial bacteria and the role successfully used worldwide to permit an effective estab- they are playing in plant growth promotion via direct and lishment of the nitrogen-fixing symbiosis with leguminous indirect mechanisims. The further elucidation of different crop plants (Bottomley and Maggard 1990; Bottomley and mechanisms involved will help to make these bacteria a Dughri 1989). On the other hand, non-symbiotic nitrogen- valuable partner in future agriculture. Ann Microbiol (2010) 60:579–598 581 Symbiotic N -fixing bacteria et al. 2003;Hayat 2005; Hayat et al. 2008a, b). In many low input grassland systems, the grasses depend on the N fixed Nitrogen is required for cellular synthesis of enzymes, by the legume counterparts for their N nutrition and protein proteins, chlorophyll, DNA and RNA, and is therefore synthesis, which is much needed for forage quality in important in plant growth and production of food and feed. livestock production (Paynel et al. 2001; Hayat and Ali For nodulating legumes, nitrogen is provided through 2010). In addition to N -fixation in legumes, Rhizobia such symbiotic fixation of atmospheric N by nitrogenase in as species of Rhizobium and Bradyrhizobium produce rhizobial bacteroids. This process of biological nitrogen molecules (auxins, cytokinins, abscicic acids, lumichrome, fixation (BNF) accounts for 65% of the nitrogen currently rhiboflavin, lipochitooligosaccharides and vitamins) that utilized in agriculture, and will continue to be important in promote plant growth (Hardarson 1993; Herridge et al. future sustainable crop production systems (Matiru and 1993; Keating et al. 1998;Hayat andAli 2004; Hayat et al. Dakora 2004). Important biochemical reactions of BNF 2008a, b). Their colonization and infection of roots would occur mainly through symbiotic association of N2-fixing also be expected to increase plant development and grain microorganisms with legumes that converts atmospheric yield (Kloepper and Beauchamp 1992;Dakora 2003; elemental nitrogen (N2) into ammonia (NH3) (Shiferaw et Matiru and Dakora 2004). Other PGPR traits of Rhizobia al. 2004). Rhizobia (species of Rhizobium, Mesorhizobium, and Bradyrhizobia include phytohormone production Bradyrhizobium, Azorhizobium, Allorhizobium and Sino- (Chabot et al. 1996a, b; Arshad and Frankenberger rhizobium) form intimate symbiotic relationships with 1998), siderophore release (Plessner et al. 1993;Jadhav legumes by responding chemotactically to flavonoid mole- et al. 1994), solubilization of inorganic phosphorus (Abd- cules released as signals by the legume host. These plant Alla 1994a;Chabotet al. 1996a) and antagonism against compounds induce the expression of nodulation (nod) genes plant pathogenic microorganisms (Ehteshamul-Haque and in Rhizobia, which in turn produce lipo-chitooligosaccharide Ghaffar 1993). A number of researchers have experimen- (LCO) signals that trigger mitotic cell division in roots, tally demonstrated the ability of Rhizobia to colonize roots leading to nodule formation (Dakora 1995, 2003; Lhuissier of non-legumes and localize themselves internally in tissues, et al. 2001; Matiru and Dakora 2004). Nodules—the sites for including the xylem (Spencer et al. 1994). Applying symbiotic nitrogen fixation—are formed as a result of series Bradyrhizobium japonicum to radish significantly increased of interactions between Rhizobia and leguminous plants. plant dry matter, by 15% (Antoun et al. 1998). Naturally- However, there are number of factors which affect the occurring Rhizobia, isolated from nodules of some tropical nodulation on legume roots including host–microsymbiont legumes, have also been shown to infect roots of many compatibility, physicochemical conditions of the soil and the agricultural species such as rice, wheat and maize via cracks presence of both known and unknown bio-molecules such as made by emerging lateral roots (Webster et al. 1997). In a flavonoides, polysaccharides and hormones (Tisdale et al. study with maize, Chabot et al. (1996b) used biolumines- 1990; Zafar-ul-Hye et al. 2007). It is a molecular dialogue cence from Rhizobium leguminosarum bv. phaseoli strain between the host plant and a compatible strain of Rhizobium harboring lux genes to visualize in situ colonization of roots which serves as an initiate of the development of nodules by Rhizobia, as well as to assess the efficiency with which (Murray et al. 2007). The rhizobial infection begins when the these bacteria infected maize roots. These observations were bacteria enters into roots in a host-controlled manner consistent with findings on maize root colonization and (Limpens et al. 2003). Rhizobium becomes trapped in a infection by Rhizobia reported by Schloter et al. (1997)and cavity formed by curling of root hair. The root hair plasma Yanni et al. (2001). membrane invaginates the cavity, and a tube-like structure is The success of laboratory studies in infected cereal roots formed by which Rhizobium enters the plant and reaches the with Rhizobia led to the hypothesis that during legume– base of the root hair. Consequently, the infection thread reaches cereal rotations and/or mixed intercropping Rhizobia are a nodule primordium in the cortex of the root that develops into brought into closer contact with cereal roots, and this a nodule upon release of the Rhizobium (Limpens et al. 2003). probably results in non-legume root infection by native Sometimes, no nodulation occurs in spite of inoculation with rhizobial populations in the soil. Yanni et al. (1997) certain rhizobial cultures, because the strains used in such isolated Rhizobium leguminosarum bv. trifolii as a natural cases become exopolysaccharide-deficient due to mutation or endophyte from roots of rice in the Nile delta. Because any unspecified reason (van Rhijn et al. 2001). rice has been grown in rotation with berseem clover for Rhizobium–legume symbiosis has been examined exten- about seven centuries in the Nile delta, this probably sively. The N fixed by Rhizobia in legumes can also benefit promoted closer rhizobial affinity to this cereal as a “host associated non-legumes via direct transfer of biologically plant”. This hypothesis is re-enforced by the fact that fixed N to cereals growing in intercrops (Snapp et al. 1998) population of clover-nodulating Rhizobia isolated from rice 7 −1 or to subsequent crops rotated with symbiotic legumes (Shah could occur up to 2.5×10 cell g fresh weight of root, 582 Ann Microbiol (2010) 60:579–598 concentrations similar to those obtained for bacteroids in wheat, maize, sugarcane and cotton), and significantly legume root nodules. Chaintreuil et al. (2000)similarly increase their vegetative growth and grain yield (Kennedy isolated photosynthetic Bradyrhizobia from roots of the et al. 2004). Azotobacter species (Azotobacter vinelandii African brown rice, Oryza glaberrima, which generally and Azotobacter chroococcum) are free-living heterotrophic grows in the same wetland as Aeschynomene sensitiva,a diazotrophs that depend on an adequate supply of reduced stem-nodulated legume associated with photosynthetic strains C compounds such as sugars for their energy source of Bradyrhizobium. Again, this may well suggest co- (Kennedy and Tchan 1992). Their activity in rice culture evolution of Aeschynomene, Bradyrhizobia and wild geno- can be increased by straw application (Kanungo et al. 1997), type of African brown rice. But whether these Bradyrhizobia presumably as a result of microbial breakdown of cellulose affect growth of O. glaberrima plant has not been deter- into cellobiose and glucose. Yield of rice (Yanni and El- mined. Besides rice, Rhizobia have also been isolated as Fattah 1999), cotton (Iruthayaraj 1981; Patil and Patil 1984; natural endophyets from roots of other non-legumes species Anjum et al. 2007), and wheat (Soliman et al. 1995;Hegazi such as cotton, sweet corn (Mclnroy and Kloepper 1995), et al. 1998; Barassi et al. 2000) increased with the maize (Martinez-Romero et al. 2000), wheat (Biederbeck et application of Azotobacter. In contrast to Azotobacter, al. 2000) and canola (Lupwayi et al. 2000) either grown in Clostridia are obligatory anaerobic heterotrophs only capable rotation with legumes or in a mixed cropping system of fixing N in the complete absence of oxygen (Kennedy involving symbiotic legumes. Rhizobial attachment to roots and Tchan 1992; Kennedy et al. 2004). Clostridia can usually of asparagus (Asparagus officinalis L), oat (AvenasativaL.), be isolated from rice soils (Elbadry et al. 1999), and their rice (Oryza sativa), and wheat (Triticum aestivum)has also activity also increased after returning straw to fields, raised been reported by Terouchi and Syono (1990). Wiehe and the C to N ratio in the soil. Holfich (1995) demonstrated that the strain R39 of Rhizobium Beneficial effects of inoculation with Azospirillum on leguminosarum bv. trifolii, multiplied under field conditions wheat yields in both greenhouse and field conditions have in the rhizosphere of host legumes (lupin and pea) as well as been reported (Hegazi et al. 1998; El Mohandes 1999; non-legumes including corn (Zea mays), rape (Brassica napus Ganguly et al. 1999). Strains of Azospirillum, a nitrogen- L) and wheat (Triticum aestivum). The effect of Rhizobium fixing organism living in close association with plants in leguminosarum bv. trifolii on non-legume plant growth has the rhizosphere. Azospirillum species are aerobic hetero- been reported to be similar to Pseudomonas fluorescens as trophs that fix N under microaerobic conditions (Roper PGPR in its colonization on certain plant roots (Hoflich et al. and Ladha 1995) and grow extensively in the rhizosphere 1994; 1995; Hoflich 2000). The plant growth promoting of gramineous plants (Kennedy and Tchan 1992; Kennedy ability of Rhizobia inoculation varies with soil properties and et al. 2004). The Azospirillum–plant association leads to crop rotation (Hilali et al. 2000; 2001). Inoculation response enhancd development and yield of different host plants to Bradyrhizobium largely depends on the soil moisture, (Fallik et al. 1994). This increase in yield is attributed available N, yield potential of the crop, and the abundance mainly to an improvement in root development by an and effectiveness of native Rhizobia (Venkateswarlu et al. increase in water and mineral uptake, and to a lesser extent 1997). In trials conducted in arid areas on legumes like guar biological N -fixation (Okon and Labandera-Gonzalez (Cyamopsis tetragonoloba L. Taub), moth (Vigna acontifolia) 1994; Okon and Itzigsohn 1995). Azospirillum brasilense and mung (Vigna radiata), inoculation gave up to 10–25% shows both chemotaxis and chemokinesis in response to yield benefits with normal rainfall (Rao 2001). Leelahawonge temporal gradient of different chemoeffectors, thereby et al. (2010) isolated root nodule bacteria from the medicinal increasing the chance of root–bacterial interactions. Phyto- legume Indigofera tinctoria and reported a new legume hormones synthesized by Azospirillum influence the host symbiont related to Pseudoalteromonas from the gamma root respiration rate, metabolism and root proliferation and class of proteobactreia. The partial nifHgene of Pseudoalter- hence improve mineral and water uptake in inoculated omonas (strain DASA 57075) had 96% similarity with nifH plants (Okon and Itzigsohn 1995). Azospirillum lipoferum gene of a member of Bradyrhizobium. The partial nodC gene and Azospirillum brasilense have been isolated from roots of Pseudoalteromonas DASA 57075 also had 88% similarity and stems of rice and sugar cane plants (Ladha et al. 1982; with nodC gene of several Rhizobia including Sinorhizobium, James et al. 2000; Reis et al. 2000) while Azospirillum Bradyrhizobium and Mesorhizobium amazonese has been isolated from the roots of rice (Pereira et al. 1988), and root and stems of sugar cane (Reis et al. 2000). In greenhouse studies, inoculation with Azospirillum −1 Non-symbiotic N -fixing bacteria lipoferum increased rice yield up to 6.7 g plant (Mirza et al. 2000). Balandreau (2002) found in a field experiment −1 A range of plant growth promoting rhizobacteria (PGPR) that estimated yield increased was around 1.8 t ha due to participate in interaction with C3 and C4 plants (e.g., rice, inoculation with Azospirillum lipoferum. Wheat grain yield Ann Microbiol (2010) 60:579–598 583 −1 was increased by up to 30% (Okon and Labandera-Gonzalez found capable of saving 25–30 kgN ha of fertilizer. The 1994) by inoculation with Azospirillum brasilense. Plant species B. glumae causes grain and seedling rot of rice inoculation with Azospirillum brasilense promoted greater (Nakata 2002). Another species, B. cepacia, can be hazard- 3- + uptake of NO ,K and H PO in corn, sorghum and wheat ous to human health (Balandreau 2002), so appropriate care 2 4 (Zavalin et al. 1998;Saubidetet al. 2000). Inoculation with and risk-reducing techniques should be employed while Azospirillum brasilense significantly increases cotton plant isolating and culturing species of Burkholderia (Kennedy et height and dry matter under greenhouse conditions (Bashan al. 2004). B. brasilensis is an endophyte of roots, stems and 1998). leaves of sugarcane plant while B. tropicalis is confined to its Soil applications with Azospirillum can significantly roots and stems (Reis et al. 2000). There is also evidence that increase cane yield in both plant and ratoon crops in the these organisms can produce substances antagonistic to field (Shankariah and Hunsigi 2001). The PGPR effects nematodes (Meyer et al. 2000). also increase N and P uptake in field trials (Galal et al. Several species of family Enterobacteriaceae include 2000; Panwar and Singh 2000), presumably by stimulating diazotrophs, particularly those isolated from the rhizosphere greater plant root growth. Substantial increases in N uptake of rice. These enteric genera containing some examples of by wheat plants and grain were observed in greenhouse diazotrophs with PGP activity include Klebsiella, Enter- trials with inoculation of Azospirillum brasilense (Islam et obacter, Citrobacter, Pseudomonas and probably several al. 2002). N tracer techniques showed that Azospirillum others yet unidentified (Kennedy et al. 2004). Klebsiella brasilense and Azospirillum lipoferum contributed 7–12% pneumoniae, Enterobacter cloacae, Citrobacter freundii of wheat plant N by BNF (Malik et al. 2002). Inoculation and Pseudomonas putida or Pseudomonas fluorescens are with Azospirillum brasilense significantly increases N also examples of such plant-associated bacteria. Herbaspir- −1 contents of cotton up to 0.91 mg plant (Fayez and Daw illum is an endophyte which colonises sugarcane, rice, 1987). Inoculation with Azospirillum also significantly maize, sorghum and other cereals (James et al. 2000). It can increased N content of sugarcane leaves in greenhouse fix 31–45% of total plant N in rice (30-day-old rice experiments (Muthukumarasamy et al. 1999). Azospirillum seedling) N from the atmosphere (Baldani et al. 2000). is also capable of producing antifungal and antibacterial The estimated N fixation by Herbaspirillum was 33–58 mg −1 compounds, growth regulators and siderophores (Pandey tube under aseptic conditions (Reis et al. 2000). In a and Kumar 1989). Acetobacter (Gluconacetobacter) diaz- greenhouse study, inoculation with Herbaspirillum in- −1 otrophicus is another acid-tolerant endophyte which grows creased rice yield significantly up to 7.5 g plant (Mirza best on sucrose-rich medium (James et al. 1994; Kennedy et al. 2000). These authors quantified BNF by different et al. 2004). Studies confirmed that up to 60–80% of strains of Herbaspirillum in both basmati and super basmati −1 −1 sugarcane plant N (equivalent to over 200 kgN ha year ) rice. The %N (N derived from the atmosphere) values were was derived from BNF and Azospirillum diazotrophicus is 19.5–38.7, and 38.1–58.2 in basmati and super basmati, apparently responsible for much of this BNF (Boddey et al. respectively. Herbaspirillum seropedicae also acts as an 1991). The Acetobacter-sugarcane system has now become endophytic diazotroph of wheat plants (Kennedy and Islam an effective experimental model and the diazotrophic 2001), colonizing wheat roots internally between the cells. character (nif ) is important component of this system Herbaspirillum seropedicae is also found in roots and (Lee et al. 2002). Reinhold-Hurek et al. (1993) studied a stems of sugarcane plant while Herbaspirillum rubrisubal- strain of the endophytic Gram-negative N -fixing bacterium bicans is an obligate endophyte of roots, stems and leaves Azoarcus sp. BH72, originally isolated from Kallar grass (Reis et al. 2000). Herbaspirilla can also colonize maize (Leptochloa fusa Kunth) growing in the saline-sodic soils plants endophytically and fix N , in addition to sugarcane typical of Pakistan. Azoarcus spp. also colonise grasses, and wheat (James et al. 2000). such as rice, in both laboratory and field conditions (Hurek et al. 1994). In rice roots, the zone behind the meristem was most intensively colonized and response of rice roots to Phosphorus-solubilizing bacteria inoculation with Azoarcus sp. BH72 in aseptic system was cultivar-dependent (Reinhold-Hurek et al. 2002). The genus Phosphorus (P) is one of the major essential macronutrients Burkholderia comprises 67 validly published species, with for plant growth and development (Ehrlich 1990). It is −1 several of these including Burkholderia vietnamiensis, B. present at levels of 400–1,200 mgkg of soil. Phosphorus kururiensis, B. tuberum and B. phynatum being capable of exists in two forms in soil, as organic and inorganic fixing N (Estrada-delos Station et al. 2001; Vandamme et phosphates. To convert insoluble phosphates (both organic al. 2002). When B. vietnamiensis was used to inoculate rice and inorganic) compounds in a form accessible to the plant in a field trial, it increased grain yields significantly up to is an important trait for a PGPR in increasing plant yields −1 8tha (Tran Vân et al. 2000). In field trials, this strain was (Igual et al. 2001; Rodríguez et al. 2006). The concentration 584 Ann Microbiol (2010) 60:579–598 of soluble P in soil is usually very low, normally at levels of al. 1991; Rodríguez and Fraga 1999), phytase (Richardson 1 ppm or less (Goldstein 1994). The plant takes up several P and Hadobas 1997), phosphonoacetate hydrolase (McGrath −2 forms but major part is absorbed in the forms of HPO4 or et al. 1998), D-α-glycerophosphatase (Skrary and Cameron −1 H PO . The phenomenon of P fixation and precipitation in 1998) and C-P lyase (Ohtake et al. 1996). Activity of 2 4 soil is generally highly dependent on pH and soil type. various phosphatases in the rhizosphere of maize, barley, Several reports have documented microbial P release from and wheat showed that phosphatase activity was consider- organic P sources (McGrath et al. 1995; Ohtake et al. 1996; able in the inner rhizosphere at acidic and neutral soil pH McGrath et al. 1998; Rodríguez and Fraga 1999). Bacterial (Burns 1983). Soil bacteria expressing a significant level of strains belonging to genera Pseudomonas, Bacillus, Rhizo- acid phosphatases include strains from the genus Rhizobium bium, Burkholderia, Achromobacter, Agrobacterium, Micro- (Abd-Alla 1994a, b), Enterobacter, Serratia, Citrobacter, ccocus, Aerobacter, Flavobacterium and Erwinia have the Proteus and Klebsiella (Thaller et al. 1995a), as well as ability to solubilize insoluble inorganic phosphate (mineral Pseudomonas (Gügi et al. 1991) and Bacillus (Skrary and phosphate) compounds such as tricalcium phosphate, dical- Cameron 1998). Four strains, namely Arthrobacter ureafa- cium phosphate, hydroxyl apatite and rock phosphate ciens, Phyllobacterium myrsinacearum, Rhodococcus (Goldstein 1986; Rodríguez and Fraga 1999; Rodríguez et erythropolis and Delftia sp. have been reported for the first al. 2006). Strains from genera Pseudomonas, Bacillus and time by Chen et al. (2006) as phosphate-solubilizing Rhizobium are among the most powerful phosphate solubil- bacteria (PSB) after confirming their capacity to solubilize izers, while tricalcium phosphate and hydroxyl apatite seem considerable amounts of tricalcium phosphate in the to be more degradable substrates than rock phosphate (Arora medium by secreting organic acids. There are also more and Gaur 1979; Illmer and Schinner 1992;Halder and reports on phosphate solubilization by Rhizobium (Halder et Chakrabarty 1993; Rodríguez and Fraga 1999;Banerjee et al. 1990, 1991;Abd-Alla 1994a, b; Chabot et al. 1996a, b) al. 2006). The production of organic acids especially and the non-symbiotic nitrogen fixer, Azotobacter (Kumar et gluconic acid seems to be the most frequent agent of mineral al. 2001). The efficacy of a strain of Mesorhizobium phosphate solubilization by bacteria such as Pseudomonas mediterraneum to enhance the growth and phosphorous sp., Erwinia herbicola, Pseudomonas cepacia and Burkhol- content in chickpea and barley plants was assessed in a soil deria cepacia (Rodríguez and Fraga 1999). Another organic with and without addition of phosphates in a growth acid identified in strains with phosphate-solubilizing ability chamber (Peix et al. 2001). The results show that strain is 2-ketogluconic acid, which is present in Rhizobium PECA21 was able to mobilize phosphorous efficiently in leguminosarum (Halder et al. 1990), Rhizobium meliloti plants when tricalcium phosphate was added to soil. The (Halder and Chakrabarty 1993), Bacillus firmus (Banik and effectiveness of strains of Rhizobia used in inoculation of a Dey 1982), and other unidentified soil bacteria (Duff and soil should not be based only on their fixation potential, Webley 1959). Strains of Bacillus licheniformis and B. since these bacteria can also increase plant growth by means amyloliquefaciens were found to produce mixtures of lactic, of other mechanisms including the phosphate solubilization isovaleric, isobutyric, and acetic acids. Other organic acids, (Peix et al. 2001). The phosphate-solubilizing activity of such as glycolic acid, oxalic acid, malonic acid, succinic Rhizobium (e.g., Rhizobium/bradyrhizobium), was associated acid, citric acid and propionic acid, have also been identified with the production of 2-ketogluconic acid which was among phosphate solubilizers (Illmer and Schinner 1992; abolished by the addition of NaOH, indicating that the (Banik and Dey 1982;Chen et al. 2006). Goldstein (1994, phosphate-solubilizing activity of this organism was entirely 1995) has proposed that the direct periplasmic oxidation of due to its ability to reduce pH of the medium (Halder and glucose to gluconic acid, and often 2-ketogluconic acid, Chakrabarty 1993). However, detailed biochemical and forms metabolic basis of the mineral phosphate solubilization molecular mechanisms of phosphate solubilization of sym- phenotype in some Gram-negative bacteria. Alternative biotic nodule bacteria need to be investigated. De Freitas et possibilities other than organic acids include the release of al. (1997) isolated 111 strains from plant rhizospheric soil, H to the outer surface in exchange for cation uptake or and a collection of nine bacteria (PGPR) were screened for ATPase which can constitute alternative ways, with the help P-solubilization in vitro. The P-solubilizing isolates were of H translocation, for solubilization of mineral phosphates identified as two Bacillus brevis strains, Bacillus mega- (Rodríguez and Fraga 1999). terium, B. polymyxa, B. sphaericus, B. thuringiensis and Soil also contains a wide range of organic substrates, Xanthomonas maltophilia (PGPR strains R85). In addition, which can be a source of P for plant growth. To make this phosphate (P)-solubilizing bacteria such as Bacillus and form of P available for plant nutrition, it must be Paenibacillus (formerly Bacillus) sp. have been applied to hydrolyzed to inorganic P. Mineralization of most organic soils to enhance the phosphorus status of plant (Van Veen et phosphorous compounds is carried out by means of al. 1997). The beneficial effects of PSB on plant growth enzymes like phosphatase (phosphohydrolases) (Gügi et varied significantly depending on environmental conditions, Ann Microbiol (2010) 60:579–598 585 bacterial strain, host plant and soil conditions (Şahin et al using the broad-host range vector pRK293 (Fraga et al. 2004; Çakmakçietal. 2006). The most common mechanism 2001). An increase in extracellular phosphatase activity of used by microorganisms for solubilizing tri-calcium phos- the recombinant strain was achieved. The ability of plants to phates seems to be acidification of the medium via obtain phosphorus directly from phytate (the primary source biosynthesis and release of a wide variety of organic acids of inositol and the major stored form of phosphate in plant (Rodríguez and Fraga 1999; Igual et al 2001; Goldstein and seeds and pollen) is very limited. However, the growth and Krishnaraj 2007;Goldstein 2007;Delvasto et al. 2008). phosphorus nutrition of Arabidopsis plants supplied with Genetic manipulation of phosphate-solubilizing bacteria phytate was improved significantly when they were geneti- is another way to enhance their ability for plant growth cally transformed with the phytase gene. Thermally stable improvement (Rodríguez and Fraga 1999; Rodríguez et al. phytase genes (phy) from Bacillus sp. DS11 (Kim et al. 2006). This may include cloning gene(s) involved in both 1998)and from Bacillus subtilis VTT E-68013 (Kerovuo et mineral and organic phosphate solubilization, followed by al. 1998) have been cloned. Acid phosphatase/phytase genes their expression in selected rhizobacterial strains (Rodríguez from Escherichia coli (appA and appA2 genes) have also et al. 2006). Several attempts have been made to identify and been isolated and characterized (Golovan et al. 2000; characterize the genes involved for P uptake and its Rodríguez et al. 1999). Neutral phytase genes have been transportation (Rossolini et al. 1998; Shenoy and Kalagudi recently cloned from Bacillus licheniformis (Tye et al. 2002). 2005). Apart from genes, quantitative trait loci (QTL) A phyA gene has been cloned from the FZB45 strain of governing maize and barley yield under P-deficient con- Bacillus amyloliquefaciens isolated from a group of several ditions have also been identified (Kajar and Jensen 1995). Bacillus having plant growth promoting activity (Idriss et al. Goldstein and Liu (1987) were the first to clone a gene 2002). involved in mineral phosphate solubolization from the Gram- negative bacteria Erwinia herbicola. Expression of this gene allowed production of GA in Escherichia coli HB101 and Other mechanisms of plant growth promotion conferred the ability to solubilize hydroxyl apatite. Another type of gene (gabY) involved in GA production and mineral Rhizosphere bacteria may improve the uptake of nutrients to phosphate solubolization was cloned from Pseudomonas plants and/or produce plant growth promoting compounds. cepacia (Babu-Khan et al. 1995). Genes for four major P They also protect plant root surfaces from colonization by metabolic enzymes have been investigated (Valverde et al. pathogenic microbes through direct competitive effects and 1999). The cytosolic GAPDH is coded by the nuclear gene production of antimicrobial agents. These bacteria can GapC, whereas the chloroplastic GAPDH is encoded by the indirectly or directly affect plant growth (Kloepper et al. nuclear genes GapA and GapB. The nuclear GapN encodes 1989;Kloepper 1993, 1994;Glick 1995; Mantelin and the cytosolic GAPDHN. The PGK is coded by nuclear gene Touraine 2004). pgk (Serrano et al. 1993). These cloned genes are an Symbiotic and non-symbiotic bacteria may promote important source of material for genetic manipulation of plant growth directly through production of plant PGPR strains for this trait. Some of them code for acid harmones (Dangar and Basu 1987;Lynch 1990;Arshad phosphatase enzymes that are capable of performing well in and Frankenberger 1991, 1993;Glick 1995;Garcíade soil. For example, acpA gene isolated from Francisella Salamone et al. 2001; Gutiérrez-Mañero et al. 2001; tularensis expresses an acid phosphatase with optimum Persello-Cartieaux et al. 2003; Dobbelaere et al. 2003; activity at pH 6, with a wide range of substrate specificity Vivas et al. 2005) and other PGP activities (Dobbelaere et al. (Reilly et al. 1996). Also, genes encoding nonspecific acid 2003). Plant growth promoting rhizobacteria (PGPR) syn- phosphatases class A (PhoC) and class B (NapA) isolated thesizes and exports phytohormones which are called plant from Morganella morganii are very promising (Thaller et al. growth regulators (PGRs). These PGRs may play regulatory 1994; 1995b). Among rhizobacteria, a gene from Burkhol- role in plant growth and development. PGRs are organic deria cepacia that facilitates phosphatase activity has been substances that influence physiological processes of plants at isolated (Rodríguez et al. 2000). This gene codes for an outer extremely low concentrations (Dobbelaere et al. 2003). membrane protein that enhances synthesis in the absence of Bacteria known to produce PGRs are listed in Table 1. soluble phosphates inthe medium, and could be involved in P There are five classes of well-known PGRs, namely auxins, transport to the cell. Besides, cloning of two nonspecific gibberellins, cytokinins, ethylene and abscisic acid (Zahir et periplasmic acid phosphatase genes (napD and napE) from al. 2004). Much attention has been given on the role of Rhizobium (Sinorhizobium) meliloti has been accomplished phytohormone auxin. The physiologically most active auxin (Deng et al. 1998, 2001). The napA phosphatase gene from in plants is indole-3-acetic acid (IAA), which is known to the soil bacterium Morganella morganii was transferred to stimulate both rapid (e.g., increases in cell elongation) and Burkholderia cepacia IS-16, a strain used as a biofertilizer, long-term (e.g., cell division and differentiation) responses in 586 Ann Microbiol (2010) 60:579–598 Table 1 Production of plant growth regulators (PGRs) by rhizobacteria and crop responses PGPR PGRs Crops Responses Reference Kluyvera ascorbata Siderophores, Canola, Both strains decreased some plant growth Burd et al. SUD 165 indole-3-acetic acid tomato inhibition by heavy metals (nickel, lead, zinc) (2000) Rhizobium leguminosarum Indole-3-acetic acid Rice Inoculation with R. leguminosarum had significant Biswas et al. growth promoting effects on rice seedlings. (2000) Rhizobium leguminosarum Indole-3-acetic acid Rice Growth promoting effects upon inoculation on Dazzo et al. axenically grown rice seedlings were observed (2000) Azotobacter sp. Indole-3-acetic acid Maize Inoculation with strain efficient in IAA production had Zahir et al. significant growth promoting effects on maize seedlings. (2000) Rhizobacterial isolates Auxins Wheat, rice Inoculation with rhizobacterial isolates had significant Khalid et al. growth promoting effects on wheat and rice (2001) Rhizobacteria (unidentified) Indole-3-acetic acid Brassica Significant correlation between auxin production by PGPR Asghar et al. in vitro and growth promotion of inoculated rapeseed (2002) seedlings in the modified jar experiments were observed Rhizobacteria (unidentified) Indole-3-acetic acid Wheat, rice Rhizobacterial strains active in IAA production had Khalid et al. relatively more positive effects on inoculated seedlings. (2001) Pseudomonas fluorescens Siderophores, Groundnut Involvement of ACC deaminase and siderophore production Dey et al. indole-3-acetic acid promoted nodulation and yield of groundnut (2004) Rhizobacteria (Unidentified) Auxin, indole-3-acetic acid, Wheat Strain produced highest amount of auxin in non-sterilized Khalid et al. acetamide soil and caused maximum increase in growth yield (2003, 2004) Azospirillum brasilense Indole-3-acetic acid, Rice All the bacterial strains increased rice grain yield over Thakuria et al. A3, A4, A7, A10, CDJA uninoculated control (2004) Bacillus circulans P2, Bacillus sp. P3,Bacillus magaterium P5, Bacillus. Sp. Psd7 Streptomyces anthocysnicus Pseudomonas aeruginosa Psd5 Pseudomonas pieketti Psd6, Pseudomonas fluorescens MTCC103, Azospirillum lipoferum Wheat Promoted development of wheat root system even under crude Muratova et al. strains 15 oil contamination in pot experiment in growth chamber (2005) Pseudomonas denitrificans Auxin Wheat, All the bacterial strains had been found to increase plant Egamberdiyeva Pseudomonas rathonis maize growth of wheat and maize in pot experiments (2005) -1 Azotobacter sp. Indole-3-acetic acid Sesbenia, Increasing the concentration of tryptophane from 1 mgml Ahmad et al. -1 Pseudomonas sp. mung bean to 5 mgml resulted in decreased growth in both crops (2005) Pseudomonas sp. Indole-3-acetic acid Wheat A combined bio-inoculation of diacetyl-phloreglucinol producing Roesti et al. PGPR and AMF and improved the nutritional quality of wheat grain (2006) Bacillus cereus RC 18, Indole-3-acetic acid Wheat, All bacterial strains were efficient in indole acetic acid (IAA) Çakmakçi et al. Bacillus licheniformis RC08, spinach production and significantly increased growth of wheat and spinach (2007b) Bacillus megaterium RC07, Bacillus subtilis RC11, Bacillus. OSU-142, Bacillus M-13, Pseudomonas putida RC06, Paenibacillus polymyxa RC05 and RC14 Mesorhizobium loti MP6, Chrom-azurol, siderophore Brassica Mesorhizobium loti MP6-coated seeds enhanced seed germination, Chandra et al. (CAS), hydrocyanic acid early vegetative growth and grain yield as compared to control (2007) (HCN), indole-3-acetic acid Pseudomonas tolaasii Siderophores, Brassica PGPR strains protect canola plant against the inhibitory Dell’Amico et al. ACC23, iIndole-3-acetic acid effects of cadmium (2008) Pseudomonas fluorescens ACC9, Alcaligenes sp. ZN4, Mycobacterium sp. ACC14, Bacillus sp. Indole-3-acetic acid Rice The isolate SVPR 30, i.e. strain of Bacillus sp., proved Beneduzi et al. Paenibacillus sp. to be efficient in promoting a significant increase in the (2008) root and shoot parts of rice plants Streptomyces acidiscabies Hydroxamate Cowpea S. acidiscabies promoted cowpea growth under nickel stress Dimkpa et al. E13 siderophores (2008) Ann Microbiol (2010) 60:579–598 587 plants (Cleland 1990; Hagen 1990). IAA is the most germination, root elongation (as well as symbiotic N fixation common and best characterized phytohormone. It has been in leguminous plants) is inhibited (Jackson 1991). It has been estimated that 80% of bacteria isolated from the rhizosphere proposed that many plant growth promoting bacteria may can produce plant growth regulator IAA (Patten and Glick promote plant growth by lowering the levels of ethylene in 1996). In addition to IAA, bacteria such as Paenibacillus plants. This is attributed to the activity of enzyme 1- polymyxa and Azospirilla also release other compounds in aminocyclopropane-1-carboxylate (ACC) deaminase, which the rhizosphere, like indole-3-butyric acid (IBA), Trp and hydrolyzes ACC, the immediate biosynthesis precursor of tryptophol or indole-3-ethanol (TOL) that can indirectly ethylene in plants (Yang and Hoffman 1984). The products of contribute to plant growth promotion (Lebuhn et al. 1997; this hydrolysis, ammonia and αketobutyrate, can be used by El-Khawas and Adachi 1999). Cytokinins are other impor- the bacterium as a source of nitrogen and carbon for growth tant phytohormones usually present in small amounts in (Klee et al. 1991). In this way, the bacterium acts as a sink for biological samples, and their identification and quantification ACC and thus lowers ethylene level in plants, preventing is difficult. Nieto and Frankenberger (1990b)reportedon some of the potentially deleterious consequences of high cytokinin by using bioassays. The most noticeable effect of ethylene concentrations (Glick et al. 1998; Steenhooudt and cytokinin on plants is enhanced cell division: however, root Vanderleyden 2000; Saleem et al. 2007). PGPR with ACC- development and root hair formation is also reported deaminase trait usually give very consistent results in (Frankenberger and Arshad 1995). Plants and plant- improving plant growth and yield, and thus are good associated microorganisms have been found to contain over candidates for bio-fertilizer formulation (Shaharoona et al. 30 growth promoting compounds of the cytokinin group. It 2006a, 2006b). The role of PGPR in production of has been found that as many as 90% of microorganisms phosphataes, β-gluconase, dehydroginase, antibiotic (Hass found in the rhizosphere are capable of releasing cytokinins and Keel 2003) solubilization of mineral phosphates and when cultured in vitro (Barea et al. 1976). Nieto and other nutrients, stabilization of soil aggregates, improved soil Frankenberger (1990a, 1991) studied the effect of the structure and organic matter contents (Miller and Jastrow cytokinin precursor’s adenine (ADE) and isopentyl alcohol 2000) has been recognized. The mechanisms involved have (IA) and cytokinin-producing bacteria Azotobacter chroo- a significant plant growth promoting potential, retaining coccum on the morphology and growth of radish and maize more soil organic N and other nutrients in plant–soil systems, under in vitro, greenhouse and field conditions. They found thus reducing the need of N and P fertilizers (Kennedy et al. improvement in plant growth. A number of articles have 2004) and enhancing the release of nutrients (Lynch 1990; reported that PGPR also produced gibberellins (GAs). Nautiyal et al. 2000; Walsh et al. 2001;Dobbelaere etal. Dobbelaere et al. (2003) reported that over 89 GAs are 2003; Ladha and Reddy 2003). known to date and are numbered GA1 through GA89 in PGPR has also been used to remediate contaminated approximate order of their discovery (Frankenberger and soils (Zhuang et al. 2007; Huang et al. 2004, 2005; Arshad 1995; Arshad and Frankenberger 1998). The most Narasimhan et al. 2003) and mineralize organic compounds widely recognized gibberellin is GA3 (gibberellic acid), the in association with plants (Saleh et al. 2004). The combined most active GA in plants is GA1, which is primarily use of PGPR and specific contaminant-degrading bacteria responsible for stem elongation (Davies 1995). In addition can successfully remove complex contaminants (Huang et abscisic acid (ABA) has also been detected by radio- al. 2005). The application of certain rhizobacteria can immunoassay or TLC in supernatants of Azospirillium and increase the uptake of Ni from soils by changing its phase Rhizobium sp. cultures (Kolb and Martin 1985;Dangar and (Abou-Shanab et al. 2006). Important genera of bacteria Basu 1987; Dobbelaere et al. 2003). Primary role of ABA in used in natural and man-created bioremediation includes stomatal closure is well established, as well as its uptake by Bacillus, Pseudomonads, Methanobacteria, Ralstonia and and transport in plant, its presence in the rhizosphere coud be Deinococcus, etc. (Milton 2007). Rhodobacter can fix extremely important for plant growth under a water-stressed carbon and nitrogen from air to make biodegradable environment, such as is found in arid and semiarid climates plastics (Sasikala and Ramana 1995). Bacteria Ralstonia (Frankenberger and Arshad 1995). metallidurans (Goris et al. 2001)and Deinocococcus Ethylene is synthesized by many and perhaps all species radiodurans (Callegan et al. 2008) can tolerate high levels of bacteria (Primrose 1979). Ethylene is a potent plant of toxic metals and radioactivity, respectively. These growth regulator that affects many aspects of plant growth, bacteria can also be used to clean up pollutants in iron, development, and senescence (Reid 1987). In addition to its copper, silver and uranium mines. Specific bacteria facilitate recognition as a ripening hormone, ethylene promotes the removal of carbon, nitrogen and phosphorus compounds formation of adventious root and root hair, stimulates while others remove toxic metals, aromatic compounds, germination, and breaks dormancy of seeds (Esashi 1991). herbicides, pesticides and xenobiotics in multi-step processes However, if ethylene concentration remains high after involving both aerobic and anaerobic metabolism (Milton 588 Ann Microbiol (2010) 60:579–598 2007). The bacterium Accumulibacter phosphatis has been duced by various bacteria that promote plant growth and responsible for the removal of phosphates (Hesselmann et al. induce systemic resistance in Arabidopsis thaliana). 1999; Zhang et al. 2003). Previous research has shown the practicality of intro- Indirect plant growth promotion includes the preven- ducing PGPR into commercial peat-based substrates for tion of deleterious effects of phytopathogenic organisms vegetable production in order to increase plant vigor, (Schippers et al. 1987; Dobbelaere et al. 2003;Glick and control root diseases and increase yields (Kokalis-Burelle Pasternak 2003). This can be achieved by the production 2003; Kokalis-Burelle et al. 2002a, 2002b, 2003, 2006; of siderophores, i.e. small iron-binding molecules. In Kloepper et al. 2004). Trials conducted on muskmelon soils, iron is found predominately as ferric ions, a form (Cucumis melo) and water melon (Citrullus lanatus) that cannot be directly assimilated by microorganisms. resulted in reduction of root knot nematode disease severity Siderophore production enables bacteria to compete with with several PGPR formulations (Kokalis-Burelle et al. pathogens by removing iron from the environment (O´ 2003). Kokalis-Burelle et al. (2006) conducted field trials in Sullivan and O´Gara 1992;Persello-Cartieauxetal. 2003). Florida on bell pepper (Capsicum annuum) to monitor the Siderophore production is very common among Pseudo- population dynamics of two plant growth-promoting rhizo- monads (O´Sullivan and O´Gara 1992), Frankia (Boyer et bacteria (PGPR) strains (Bacillus subtilis strain GBO3 and al. 1999)and Streptomyces sp. (Loper and Buyer 1991) Bacillus amyloliquefaciens strain IN937a) applied in the have also been shown to produce iron-chelating com- potting media at seedling stage and at various times after pounds. Biological control of soil-borne plant pathogens transplanting to the field during the growing season. Most (Sutton and Peng 1993;Idrissetal. 2002; Chin-A-Woeng treatments reduced disease incidence in a detached leaf et al. 2003;Picardetal. 2004) and the synthesis of assay compared to control, indicating that systemic antibiotics have also been reported in several bacterial resistance was induced by PGPR treatments. Application species (O´Sullivan and O´Gara 1992;Haansuuetal. of PGPR strains did not adversely affect populations of 1999). Another mechanism by which rhizobacteria can beneficial indigenous rhizosphere bacteria including inhibit phytopathogens is the production of hydrogen fluorescent pseudomonads and siderophore-producing cyanide (HCN) and/or fungal cell wall-degrading enzymes bacterial strains. Treatment with PGPR increased pop- e.g., chitinase and ß-1, 3-glucanase (Friedlender et al. 1993; ulations of fungi in the rhizosphere but did not result in Bloemberg and Lugtenberg 2001; Persello-Cartieaux et al. increased root disease incidence. This fungal response to 2003). Although pectinolytic capability is usually associated PGPR products was likely due to an increase in with phytopathogenic bacteria, nonphytopathogenic species nonpathogenic chitinolytic fungal strains resulting from such as Rhizobium (Angle 1986), Azospirillum (Umali- application of chitosan, which is a component of the Garcia et al. 1980;Tienet al. 1981), some strains of PGPR formulation applied to the potting media. Table 2 Klebsiella pneumoniae and Yersinia (Chatterjee et al. 1978), cites important studies of biological control by PGPR and Frankia (Séguin and Lalonde 1989) are also able to against certain diseases, pathogens and insects in different degrade pectin. In general, pectinolytic enzymes play an crops. important role in root invasion by bacteria. While PGPR Inoculation of Pseudomonas fluorescens isolates have been identified within many different bacterial taxa, PGPR1, PGPR2 and PGPR4 reduced the seedling mortality most commercially developed PGPR are species of Bacillus caused by Aspergillus niger (Dey et al. 2004). Inoculation which come from endospores that confer population stability of Pseudomonas fluorescens isolates PGPR4 and PGPR5 during formulation and storage of products. Among bacilli, showed strong inhibition to Sclerotium rolfsii, and reduced strains of Bacillus subtilis are the most widely used PGPR the incidence of stem rot severity. Several Pseudomonas due to their disease-reducing and antibiotic-producing fluorescens isolates, viz. PGPR1, PGPR2 and PGPR4, also capabilities when applied as seed treatments (Brannen and produced siderophores and antifungal metabolites. Produc- Backman 1994; Kokalis-Burelle et al. 2006). Specific tion of antifungal metabolites by fluorescent pseudomonads mechanisms involved in pathogen suppression by PGPR has also been found to suppress soil-borne fungal patho- vary and include antibiotic production, substrate compe- gens on many occasions (Pal et al. 2001; Dey et al. 2004). tition, and induced systemic resistance in the host (Van There are some cases where PGPR promoted plant growth Loon et al. 1998). Flourescent pseudomonads are known in non-sterile soil by controlling fungal diseases (Cattelan et to suppress soil-borne fungal pathogens by producing al. 1999). The addition of siderophores-producing Pseudo- antifungal metabolites and by sequestering iron in the monas putida converted a fusarium-conducive soil into a rhizosphere through release of iron-chelating sidero- fusarium-suppressive soil for growth of different plants phores, and thus rendering it unavailable to other (Dey et al. 2004). Improvement in plant growth and disease organisms (Dwivedi and Johri 2003). Ryu et al. (2004) resistance to a broad array of plant pests can be accom- have identified several volatile organic compounds pro- plished using PGPR (Kloepper et al. 2004). The concept of Ann Microbiol (2010) 60:579–598 589 Table 2 Biological control by PGPR against diseases, pathogens and insects in different crops PGPR Crops Disease/pathogen/insect Reference Bacillus amyloliquefaciens strain 1 N 937a Tomato Tomato mottle virus Murphy et al. (2000) Bacillus subtilis 1 N 937b Pseudomonas fluorescens and Tobacco Tobacco necrosis virus, wild fire Park and Kloepper (2000) unidentified PGPR (Ps. syringae, Pv. tabaci) Pseudomonas aeruginosa, Bacillus subtilis Mung bean Root rot, root knot Siddiqui et al. (2001) Streptomyces marcescens 90-116, Tobacco Blue mold Zhang et al. (2003) Bacillus pumilus SE 34, Pseudomonas fluorescens 89B-61, Bacillus pumilus T4, Bacillus pasteurii C-9 Pseudomonas sp White clover Medicago Blue green aphids Acyrthosiphon kondoi Shinji Kempster et al. (2002) Bacillus sp. Cucumber Cotton aphids Aphiz gossypii Glover Stout et al. (2002) Bacillus amyloliquefaciens Pepper Myzus persicae Kokalis-Burelle et al. (2002b) strain 1 N 937a Bacillus subtilis G803 Pseudomonas sp. Groundnut Charcoal rot caused by Rhizoctonia bataticola Gupta et al. (2002) Azotobacter sp., Pseudomonas sp. Wheat Fungal biocontrol Wachowaska (2004) Bacillus licheniformis Tomato, pepper Myzus persicae Lucas et al. (2004b) Pseudomonas fluorescens Pea nut Collar rot caused by Aspergillus niger, Aspergillus flavus Dey et al. (2004) and stem rot caused by Sclerotium rolfsii Glomus mosseae, Bacillus subtilis, Strawberry Crown rot caused by Phytophothora cactorum and Vestberg et al. (2004) Pseudomonas fluorescens red steel caused by Phytophothora fragari Trichoderma harzianum, Gliocladium catenalatum Bacillus cereus MJ-1 Red pepper Myzus persicae Joo et al. (2005) Paenibacillus polymyxa E681 Sesame Fungal disease Ryu et al. (2006) Mesorhizobium loti MP6, Mustard Brassica compestris White rot Sclerotinia sclerotiorum Chandra et al. (2007) Bacillus amyloliquoefaciens, Bell pepper Green peach aphids, Myzus persicae Sluzer Herman et al. (2008) Bacillus subtilis Azospirillum brasilense Sp245 Prunus cerasifera L. clone Mr. 2/5 Rhizosphere fungi Russo et al. (2008) Rhizoctonia sp. Bacillus cereus BS 03, Pigeonpea Fusarial wilt, Fusarium udum Dutta et al. (2008) Pseudomonas aeruginosa RRLJ04 Rhizobia Pseudomonadaceae family. Pea, entil and chickpea Pythium sp. Hynes et al. (2008) Fusarium avenaceum Enterobacteriaceae family Rhizoctonia solani CKP7 introducing PGPR into the rhizosphere using the transplant establishment and disease (Dwivedi and Johri 2003). plug is based on the hypothesis that their establishment in Because typical disease control levels observed with the relatively clean environment of planting media would PGPR are less than those achieved with chemicals, it is afford them an opportunity to develop stable populations in feasible to utilize PGPR as components in integrated the seedling rhiozosphere, and that these populations would management systems that include reduced rates of chem- then persist in the field. It was also hypothesized that early icals and cultural control practices (Kokalis-Burelle et al. exposure to PGPR might precondition young plants to 2006). Attempts to identify methyl bromide, a soil resist pathogen attack after transplanting in the field. It is fumigant alternative for vegetable production, has led to well recognized that PGPR can influence plant growth and re-examination of existing soil fumigants (Gilreath et al. resistance to pathogens (Cleyet-Marcel et al. 2001). 2001), such as 1,3-D, metam sodium and chloropicrin, and However, it is necessary to establish a greater under- development of new broad-spectrum biocides, such as standing of the dynamics of applied beneficial organisms methyl iodide and propargyl bromide (Ohr et al. 1996; under field conditions in order to optimize their applica- Noling and Gilreath 2001), as well as increasing interest in tion method and timing. It is also important to under- non-chemical approaches. PGPR have attracted much stand the effects of applied biocontrol strains on attention in their role in reducing plant diseases. Although populations of indigenous beneficial bacteria including their full potential has not yet been reached, the work to fluorescent pseudomonads, which commonly occur in the date is very promising. Some PGPR, especially if they are rhizosphere, and are known to suppress pathogen inoculated on seeds before planting, are able to establish 590 Ann Microbiol (2010) 60:579–598 themselves on crop roots. They use scarce resources, and Abou-Shanab RAI, Angle JS, Chaney RL (2006) Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate thereby prevent or limit the growth of pathogenic micro- and high Ni soils. Soil Biol Biochem 38:2882–2889 organisms. This is a common way in which PGPR reduce Ahmad F, Ahmad I, Khan MS (2005) Indole acetic acid production the severity of damping-off (Pythium ultimum)inmany by the indigenous isolates of Azotobacter and Flourescent crops. Even if nutrients are not limiting, establishment of pseudomonas in the presence and absence of tryptophan. Turk J Biol 29:29–34 beneficial organisms on roots limits the chance that a Alvarez MI, Sueldo RJ, Barassi CA (1996) Effect of Azospirillum on pathogenic organism that arrives later will find space to coleoptile growth in wheat seedlings under water stress. Cereal become established. Numerous rhizosphere organisms are Res Commun 24:101–107 Angle JS (1986) Pectic and proteolytic enzymes produced by fast- capable of producing compounds that are toxic to and slow-growing soybean Rhizobia. Soil Biol Biochem pathogens (plant diseases). Bacillus subtilis is one such 18:115–116 commercialized PGPR organism, and it acts against a Anjum MA, Sajjad MR, Akhtar N, Qureshi MA, Iqbal A, Jami AR, wide variety of pathogenic fungi (Banerjee et al. 2006). Hassan M (2007) Response of cotton to plant growth promoting rhizobacteria (PGPR) inoculation under different levels of nitrogen. J Agric Res 45(2):135–143 Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Conclusion Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on Soil bacteria transform atmospheric N into ammonia and are radishes (Raphanus sativus L). Plant Soil 204:57–68 Arora P, Gaur AC (1979) Microbial solubilization of different central to soil and plant health. They play a pivotal role in inorganic phosphates. Indian J Exp Biol 17:1258–1261 cycling of nutrients within the soil. The soil contains Arshad M, Frankenberger WT Jr (1991) Effects of soil properties and numerous genera of bacteria, many of which not only have trace elements on ethylene production in soils. Soil Sci 151:377– important roles in nutrient cycling but also protect crops 386 Arshad M, Frenkenberger WT Jr (1993) Microbial production of plant against diseases. Plant growth promoting rhizobacteria growth regulators. In: Meeting FB Jr (ed) Soil microbial ecology. (PGPR) benefit the growth and development of plants Dekker, New York, pp 307–347 directly and indirectly through several mechanisms. The Arshad M, Frankenberger WT Jr (1998) Plant growth regulating production of secondary metabolites, i.e. plant growth substances in the rhizosphere. Microbial production and function. Adv Agron 62:46–51 substances, changes root morphology resulting in greater Asghar HN, Zahir ZA, Arshad M, Khaliq A (2002) Relationship root surface area for the uptake of nutrients, siderophores between in vitro production of auxins by rhizobacteria and their production, antagonism to soil-borne root pathogens, phos- growth-promoting activities in brassica junceal. Biol Fertil Soils 35(23):1–237 phate solubilization, and di-nitrogen fixation. The root Babu-Khan S, Yeo C, Martin WL, Duron MR, Rogers R, Goldstein A surface area for uptake of nutrients and production of PGPR (1995) Cloning of a mineral phosphate-solubilizing gene from may help to optimize nutrient cycling in the event of stresses Pseudomonas cepacia. Appl Environ Microbiol 61:972–978 due to unsuitable weather or soil conditions. Biological Balandreau J (2002) The spermosphere model to select for plant inoculums for legumes have attracted much attention growth promoting rhizobacteria. In: Kennedy IR, Choudhury ATMA (eds) Biofertilisers in action. Rural Industries Research throughout the world. Other PGPR inoculants (Azospirillum, and Development Corporation, Canberra, pp 55–63 Azotobacter, Bacillus, Pseudomonas, etc.) are also available Baldani VLD, Baldani JI, Dobereiner J (2000) Inoculation of rice plants for a variety of crops, used alone or co-inoculating with with the endophytic diazotrophs Herbaspirillums seropidicae.Biol Rhizobium sp. These technologies have resulted in positive Fertil Soils 30:485–491 Banerjee MR, Yasmin L (2002) Sulfur oxidizing rhizobacteria: an responses under controlled (laboratory and greenhouse) innovative environment friendly soil biotechnological tool for conditions; however, natural variations make it difficult to better canola production. Proceeding of AGROENVIRON. predict how PGPR may respond when applied to field Cairo, Egypt, 2002, October 26–29, pp 1-7 conditions. PGPR must be propagated artificially to optimize Banerjee MR, Yesmin L, Vessey JK (2006) Plant growth promoting rhizobacteria as biofertilizers and biopesticides. In: Rai MK (ed) their viability and biological activity under field applications. Handbook of microbial biofertilizers. Haworth Press, New York It is also suggested that PGPR need to be reinoculated every Banik S, Dey BK (1982) Available phosphate content of an alluvial year/season as they will not live forever in the soil. soil is influenced by inoculation of some isolated phosphate- solubilizing microorganisms. Plant Soil 69:353–364 Barassi CA, Creus CM, Casanovas EM, Sueldo RJ (2000) Could Azospirillum mitigate abiotic stress effects in plants? Auburn University. Web site: http://www.ag.auburn.edu/argentina/ References pdfmanuscripts/brassi.pdf Barea JM, Navarro E, Montoya E (1976) Production of plant growth Abd-Alla MH (1994a) Solubilization of rock phosphates by regulators by rhizosphere phosphate solubilizing bacteria. J Appl Rhizobium and Bradyrhizobium. Folia Microbiol 39:53–56 Bacteriol 40:129–134 Abd-Alla MH (1994b) Use of organic phosphorus by Rhizobium Bashan Y (1998) Azospirillum plant growth-promoting strains are leguminosarum biovar. viceae phosphatases. Biol Fertil Soils nonpathogenic on tomato, pepper, cotton, and wheat. Can J 18:216–218 Microbiol 44:168–174 Ann Microbiol (2010) 60:579–598 591 Beneduzi A, Peres D, Vargas LK, Bodanese-Zanettini MH, Passaglia Chabot R, Antoun H, Kloepper JW, Beauchamp CJ (1996b) Root LMP (2008) Evaluation of genetic diversity and plant growth colonization of maize and lettuce by bioluminescent Rhizobium promoting activities of nitrogen-fixing Bacilli isolated from rice leguminosaurm biovar phaseoli. Appl Environ Microbiol fields in South Brazil. Appl Soil Ecol 39:311–320 62:2767–2772 Biederbeck VO, Lupwayi NZ, Haanson KG, Rice WA, Zentner RP Chaintreuil C, Giraud E, Prin Y, Lorquin J, Ba A, Gillis M, deLajudie (2000) Effect of long-term rotation with lentis on rhizosphere P, Dreyfus B (2000) Photosynthetic bradyRhizobia are natural ecology and on endophytic Rhizobia in wheat. Abstract of the endophytes of the African wild rice Oryza breviligulata. Appl 17th North American Conference on Symbiotic Nitrogen Environ Microbiol 66:5437–5447 Fixation. Laval University Quebec, Canada, pp 23–28, July 2000 Chandra S, Choure K, Dubey RC, Maheshwari DK (2007) Rhizosphere Biswas JC, Ladha JK, Dazzo FB, Yanni YG, Rolf BG (2000) competent Mesorhizobium loti MP6 induces root hair curling, Rhizobial inoculation influences seedling vigor and yield of rice. inhibits Sclerotinia sclerotiorum and enhances growth of Indian Agron J 90:880–886 mustard (Brassica campestris). Braz J Microbiol 38:124–130 Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant Chatterjee AK, Buchanan GE, Behrens MK, Starr MP (1978) growth promotion and biocontrol by rhizobacteria. Curr Opin Synthesis and excretion of polygaracturonic and transeliminase Plant Biol 4:343–350 in Erwinia, Yersinia, and Klebsiella species. Can J Microbiol Boddey RM, Urquiaga S, Reis V, Döbereiner J (1991) Biological nitrogen 25:94–102 fixation associated with sugar cane. Plant Soil 137:111–117 Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Bottomley PJ, Dughri MH (1989) Population size and distribution of Phosphate solubilizing bacteria from subtropical soil and their Rhizobium leguminosarum biovar trifolii in relation to total soil tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41 bacteria and soil depth. Appl Environ Microbiol 55:959–964 Chin-A-Woeng TFC, Bloemberg GV, Lugtenberg BJJ (2003) Phenazines Bottomley PJ, Maggard SP (1990) Determination of viability within and their role in biocontrol by Pseudomonas bacteria. New Phytol serotypes of a soil population of Rhizobium leguminosarum 157:503–523 biovar trifolii. Appl Environ Microbiol 56:533–540 Cleland RE (1990) Auxin and cell elongation. In: Davies PJ (ed) Plant Boyer GL, Kane SA, Alexander JA, Aronson DB (1999) Siderophore hormones and their role in plant growth and development. formation in iron-limited cultures of Frankia sp. strain 52065 and Kluwer, Dordrecht, pp 132–148 Frankia sp. strain CeSI5. Can J Bot 77:1316–1320 Cleyet-Marcel JC, Larcher M, Bertrand H, Rapior S, Pinochet X (2001) Brannen PM, Backman PA (1994) Suppression of Fusarium wilt of Plant growth enhancement by rhizobacteria. In: MorotGaudry JF cotton with Bacillus subtilis hopper box formulations. In: Ryder (ed) Nitrogen assimilation by plants: physiological, biochemicval MH, Stephens PM, Bowen GD (eds) Improving plant productivity and molecular aspects. Science Publishers, Plymouth, pp 185–197 with rhizosphere bacteria, proceedings from the third international Cocking EC (2003) Endophytic colonization of plant roots by workshop on plant growth-promoting rhizobacteria. CSIRO Press, nitrogen-fixing bacteria. Plant Soil 252(1):169–175 Adelaide, pp 83–85 Dakora FD (1995) Plant flavonoids: biological molecules for useful Brierley JA (1985) Use of microorganisms for mining metals. In: exploitation. Aust J Plant Physiol 22:7–99 Halvorson HO, Pramer D, Rogul M (eds) Engineered organisims Dakora FD (2003) Defining new roles for plant and rhizobial in the environment: scientifc issues. ASM Press, Washington, pp molecules in sole and mixed plant cultures involving symbiotic 141–146 legumes. New Phytol 158:39–49 Brown ME (1974) Seed and root bacterization. Annu Rev Phytopathol Dangar TK, Basu PS (1987) Studies on plant growth substances, 12:181–197 IAA metabolism and nitrogenase activity in root nodules of Burd G, Dixon DG, Glick BR (2000) Plant growth promoting bacteria Phaseolus aureus Roxb. var. mungo. Biol Plant 29:350–354 that decrease heavy metal toxicity in plants. Can J Microbiol Davies PJ (1995) The plant hormones: their nature, occurrence, and 46:237–245 functions. In: Davies PJ (ed) Plant hormones: physiology, biochem- Burns RG (1983) Extracellular enzyme-substrate interactions in istry, and molecular biology, 2nd edn. Kluwer, Dordrecht, pp 1–12 soil. In: Slater JH, Whittenbury R, Wimpenny JWT (eds) Davison J (1988) Plant beneficial bacteria. Biotechnology 6:282–286 Microbes in their natural environment. Cambridge University Dazzo FB, Yanni YG, Rizk R, De Bruijn FJ, Rademaker J, Squartini A, Press, Cambridge, pp 249–298 Corich V, Mateos P, Martinez-Molina E et al (2000) Progress in Burr TJ, Caesar A (1984) Beneficial plant bacteria. Crit Rev Plant Sci multinational collaborative studies on the beneficial association 2:1–20 between Rhizobium Ieguminosarum by trifolii and rice. In: Ladha Çakmakçi R, Dönmez F, AydınA, Şahin F (2006) Growth promotion of JK, Reddy PM (eds) The quest for nitrogen fixation in rice. IRR1, plants by plant growth-promoting rhizobacteria under greenhouse Los Banos, Philippines, pp 167–189 and two different field soil conditions. Soil Biol Biochem 38:1482– De Freitas JR, Banerjee MR, Germida JJ (1997) Phosphate- 1487 solubilizing rhizobacteria enhance the growth and yield but not Çakmakçi R, Erat M, Erdoğan ÜG, Dönmez MF (2007) The influence phosphorus uptake of canola (Brassica napus L.). Biol Fertil of PGPR on growth parameters, antioxidant and pentose Soils 24:358–364 phosphate oxidative cycle enzymes in wheat and spinach plants. Dell’Amico E, Cavalca L, Andreoni V (2008) Improvement of J Plant Nutr Soil Sci 170:288–295 Brassica napus growth under cadmium stress by cadmium- Callegan RP, Nobre MF, McTernan PM, John BR, Navarro-González resistant rhizobacteria. Soil Biol Biochem 40:74–84 R, McKay CP, da Costa MS, Rainey FA (2008) Description of Delvasto P, Valverde A, Ballester A, Muñoz JA, González F, Blázquez four novel psychrophilic, ionizing radiation-sensitive Deinococ- ML, Igual JM, García-Balboa C (2008) Diversity and activity of cus species from alpine environments. Int J Syst Evol Microbiol phosphate bioleaching bacteria from a high-phosphorus iron ore. 58:1252–1258 Hydrometallurgy 92:124–129 Cattelan AJ, Hartel PG, Fuhrmann JJ (1999) Screening for plant Deng S, Summers ML, Kahn ML, McDermontt TR (1998) Cloning growth rhizobacteria to promote early soybean growth. Soil Sci and characterization of a Rhizobium meliloti nonspecific acid Soc Am J 63:1670–1680 phosphatase. Arch Microbiol 170:18–26 Chabot R, Antoun H, Cescas MP (1996a) Growth promotion of maize Deng S, Elkins JG, Da LH, Botero LM, McDermott TR (2001) Cloning and lettuce by phosphate-solubilizing Rhizobium leguminosarum and characterization of a second acid phosphatase from Sinorhizobium biovar phaseoli. Plant Soil 184:311–321 meliloti strain 104A14. Arch Microbiol 176:255–263 592 Ann Microbiol (2010) 60:579–598 Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion fibre-legume-cereal system in an Aeric haplaquept. Indian J Agric and yield enhancement of peanut (Arachis hypogaea L) by Res 33:35–39 application of plant growth promoting rhizobacteria. Microbiol García de Salamone IE, Hynes RK, Nelson LM (2001) Cytokinin Res 159:371–394 production by plant growthpromoting rhizobacteria and selected Dimkpa C, Aleš S, Dirk M, Georg B, Erika K (2008) Hydroxamate mutants. Can J Microbiol 47(5):404–411 siderophores produced by Streptomyces acidiscabies E13 bind Gilreath JP, Noling JW, Mirusso J, Nance J, Eger J, Gilreath P (2001) nickel and promote growth in cowpea (Vigna unguiculata L.) Telone and herbicides: do's, don’ts, and maybe's-a primer for under nickel stress. Can J Microb 54:163–172 tomorrow's farmer. FACTS Proceedings of the IFAS, University Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth- of Florida, pp 37-40 promoting effects of diazotrophs in the rhizosphere. Crit Rev Glick BR (1995) The enhancement of plant growth by free-living Plant Sci 22:107–149 bacteria. Can J Microbiol 41:109–117 Duff RB, Webley DM (1959) 2-Ketogluconic acid as a natural Glick BR (2001) Phytoremediation: synergistic use of plants and chelator produced by soil bacteria. Chem Ind 1376-1377 bacteria to cleanup the environment. Biotechnol Adv 21(3):83– Dutta S, Mishra AK, Kuma BSD (2008) Induction of systemic 393 resistance against fusarial wilt in pigeon pea through interaction Glick BR, Pasternak JJ (2003) Plant growth promoting bacteria. In: of plant growth promoting rhizobacteria and rhizobia. Soil Biol Glick BR, Pasternak JJ (eds) Molecular biotechnology principles Biochem 40:452–461 and applications of recombinant DNA, 3rd edn. ASM Press, Dwivedi D, Johri BN (2003) Antifungals from fluorescent pseudomonads: Washington, pp 436–454 biosynthesis and regulation. Curr Sci 12:1693–1703 Glick BR, Penrose DM, Li J (1998) A model for lowering plant Egamberdiyeva D (2005) Plant growth promoting rhizobacteria ethylene concentration by plant growth promoting rhizobacteria. isolated from a calsisol in semi arid region of Uzbekistan: J Theor Biol 190:63–68 biochemical characterization and effectiveness. J Plant Nutr Soil Goldstein AH (1986) Bacterial solubilization of microbial phosphates: Sci 168:94–99 a historical perspective and future prospects. Am J Altern Agric Ehrlich HL (1990) Geomicrobiology, 2nd edn. Dekker, New York, p 646 1:51–57 Ehteshamul-Haque S, Ghaffar A (1993) Use of Rhizobia in the control Goldstein AH (1994) Involvement of the quinoprotein glucose of root diseases of sunflower, okra, soybean and mungbean. J dehydrogenase in the solubilization of exogenous mineral Phytopathol 138:157–163 phosphates by Gram negative bacteria. In: Torriani-Gorni A, Elbadry M, El-Bassel A, Elbanna K (1999) Occurrence and dynamics Yagil E, Silver S (eds) Phosphate in microorganisms: cellular and of phototrophic purple nonsulphur bacteria compared with other molecular biology. ASM Press, Washington, pp 197–203 asymbiotic nitrogen fixers in rice fields of Egypt. World J Goldstein AH (1995) Recent progress in understanding the molecular Microbiol Biotechnol 15:359–362 genetics and biochemistry of calcium phosphate solubilization by El-Khawas H, Adachi K (1999) Identification and quantification of Gram negative bacteria. Biol Agric Hortic 12:185–193 auxins in culture media of Azospirillum and Klebsiella and their Goldstein AH (2007) Future trends in research on microbial phosphate effect on rice roots. Biol Fertil Soils 28:377–381 solubilization: one hundred years of insolubility. In: Velázquez E, El Mohandes MAO (1999) The use of associative diazotrophs with Rodríguez-Barrueco C (eds) First international meeting on microbial different rates of nitrogen fertilization and compost to enhance phosphate solubilization. Springer, Dordrecht, pp 91–96 growth and N -fixation of wheat. Bulletin of Faculty of Goldstein AH, Liu ST (1987) Molecular cloning and regulation of a Agriculture, University of Cairo 50:729-753 mineral phosphate solubilizing gene from Erwinia herbicola. Esashi Y (1991) Ethylene and seed germination. In: Matoo AK, Suttle Biotechnology 5:72–74 JC (eds) The plant hormone ethylene. CRC Press, Boca Raton, Goldstein AH, Krishnaraj PU (2007) Phosphate solubilizing pp 133–157 microorganisms vs. phosphate mobilizing microorganisms: Estrada-delos Station P, Bustitio-Cristales R, Caballero-Mallado J what separates a phenotype from a trait? In: Velázquez E, (2001) Burkholderia, a genus rich in plant-associated nitrogen Rodríguez-Barrueco C (eds) First International meeting on fixers with wide environmental and geographic distribution. Appl microbial phosphate solubilization. Springer, Dordrecht, pp Environ Microbiol 67:279–2798 203–213 Fallik E, Sarig S, Okon Y (1994) Morphology and physiology of plant Golovan S, Wang G, Zhang J, Forsberg CW (2000) Characterization roots associated with Azospirillum. In: Okon Y (ed) and over production of the Escherichia coli appA encoded Azospirillum-plant associations. CRC Press, Boca Raton, pp bifunctional enzyme that exhibits both phytase and acid 77–84 phosphatase activities. Can J Microbiol 46:59–71 Fayez M, Daw ZY (1987) Effect of inoculation with different strains Goris J, De Vos P, Coenye T, Hoste B, Janssens D, Brim H, Diels L, of Azospirillum brasilense on cotton (Gossypium barbadense). Mergeay M, Kersters K, Vandamme P (2001) Classification of Biol Fertil Soils 4(9):1–95 metal-resistant bacteria from industrial biotopes as Ralstonia Fraga R, Rodríguez H, Gonzalez T (2001) Transfer of the gene campinensis sp. nov., Ralstonia metallidurans sp. nov and encoding the Nap A acid phosphatase from Morganella morganii Ralstonia basilensis. Int J Syst Evol Microbiol 51:1773–1782 to a Burkholderia cepacia strain. Acta Biotechnol 21:359–369 Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: Frankenberger WTJ, Arshad M (1995) Photohormones in soil: commonalities and distinctions in the plant-bacterium signaling microbial production and function. Dekker, New York, p 503 processes. Soil Biol Biochem 37:395–412 Friedlander AM, Welkos SL, Pitt MLM, Ezzell JW, Worsham PL, Gügi B, Orange N, Hellio F, Burini JF, Guillou C, Leriche F, Guespin- Rose KJ (1993) Postexposure prophylaxis against experimental Michel JF (1991) Effect of growth temperature on several inhalation anthrax. J Infect Dis 167:1239–1242 exported enzyme activities in the psychrotropic bacterium Galal YGM, El-Ghandour IA, Aly SS, Soliman S, Gadalla A (2000) Pseudomonas fluorescens. J Bacteriol 173:3814–3820 Non-isotopic method for the quantification of biological nitrogen Guo JH, Qi HY, Guo YH, Ge HL, Gong LY, Zhang LX (2004) Biocontrol fixation and wheat production under field conditions. Biol Fertil of tomato wilt by plant growth promoting rhizobacteria. Biol Soils 32:47–51 Control 29:66–72 Ganguly TK, Jana AK, Moitra DN (1999) An evaluation of agronomic Gupta CP, Dubey RC, Maheshwari DK (2002) Plant growth potential of Azospirillum brasilense and Bacillus megaterium in enhancement and suppression of Macrophomina phaseolina Ann Microbiol (2010) 60:579–598 593 causing charcoal rot of peanut by fluorescent Pseudomonas. Biol Bell CR, Brylinsky M, Johnson-Green P (eds) Proceedings of the Fertl Soil 35:295–301 8th international symposium on microbial ecology. Atlantic Gutiérrez-Mañero FG, Ramos-solano B, Probanza A, Mehouachi J, Canada Soc, Microbial Ecol., Halifax, Canada, pp 827-830 Tadeo FR, Talon M (2001) The plant-growth promoting Hoflich G, Wiehe W, Kohn G (1994) Plant growth stimulation by rhizobacteria Bacillus pumilus and Bacillus licheniformis inoculation with symbiotic and associative rhizosphere micro- produce high amounts of physiologically active gibberellins. organisms. Experienca 50:897–905 Physiol Plant 111:206–211 Hoflich G, Wiehe W, Hecht-Buchholz CC (1995) Rhizosphere colonization Haansuu P, Vuorela P, Haahtela K (1999) Detection of antimicrobial of different crops with growth promoting Pseudomonas and 2+ and 45Ca -transport blocking activity in Frankia culture broth Rhizobium bacteria. Microbiol Res 150:139–147 extracts. Pharm Pharmacol Lett 1:1–4 Huang XD, El-Alawi Y, Penrose DM, Glick BR, Greenberg BM Hagen G (1990) The control of gene expression by auxin. In: Davies (2004) A multiprocess phytoremediation system for removal of PJ (ed) Plant hormones and their role in plant growth and polycyclic aromatic hydrocarbons from contaminated soils. development. Kluwer, Dordrecht, pp 149–163 Environ Pollut 130:465–476 Halder AK, Chakrabarty PK (1993) Solubilization of inorganic Huang XD, El-Alawi Y, Gurska J, Glick BR, Greenberg BM (2005) A phosphate by Rhizobium. Folia Microbiol 38:325–330 multi-process phytoremediation system for decontamination of Halder AK, Mishra AK, Bhattacharya P, Chakrabarthy PK (1990) persistent total petroleum hydrocarbons (TPHs) from soils. Solubilization of rock phosphate by Rhizobium and Bradyrhizobium. Microchem J 81:139–147 J Gen Appl Microbiol 36(8):1–92 Hurek T, Reinhold-Hurek B, Van Montagu M, Kellenberger E (1994) Halder AK, Misra AK, Chakrabarty PK (1991) Solubilization of inorganic Root colonization and systemic spreading of Azoarcus sp. strain phosphates by Bradyrhizobium. Indian J Exp Biol 29:28–31 BH72 in grasses. J Bacteriol 176:1913–1923 Hardarson G (1993) Methods for enhancing symbiotic nitrogen Hynes RK, Leung GCY, Hirkala DLM, Nelson LM (2008) Isolation, fixation. Plant Soil 152:1–17 selection, and characterization of beneficial rhizobacteria from Hass D, Keel C (2003) Regulation of antibiotic production in root- pea, lentil and chickpea grown in western Canada. Can J Microb colonizing Pseudomonas sp. and relevance for biological control 54:248–258 of plant disease. Annu Rev Phytopathol 41:117–153 Idriss EE, Makarewicz O, Farouk A, Rosner K, Greiner R, Bochow H, Hayat R (2005) Sustainable legume cereal cropping system through Richter T, Borriss R (2002) Extracellular phytase activity of management of biological nitrogen fixation in Pothwar. PhD Bacillus amyloliquefaciens FZB45 contributes to its plant- Dissertation. PMAS Arid Agriculture University, Rawalpindi, growth-promoting effect. Microbiology 148:2097–2109 Pakistan Igual JM, Valverde A, Cervantes E, Velázquez E (2001) Phosphate- Hayat R, Ali S (2004) Potential of summer legumes to fix nitrogen solubilizing bacteria as inoculants for agriculture: use of updated and benefit wheat crop under rainfed condition. J Agronomy molecular techniques in their study. Agronomie 21:561–568 3:273–281. Illmer P, Schinner F (1992) Solubilization of inorganic phosphates by Hayat R, Ali S (2010) Nitrogen fixation of legumes and yield of wheat microorganisms isolated from forest soil. Soil Biol Biochem under legumes-wheat rotation in Pothwar. Pak J Bot 42(3): in press 24:389–395 Hayat R, Ali S, Siddique MT, Chatha TH (2008a) Biological nitrogen Iruthayaraj MR (1981) Let Azotobacter supply nitrogen to cotton. fixation of summer legumes and their residual effects on Intensive Agric 19-23 subsequent rainfed wheat yield. Pak J Bot 40(2):711–722 Islam N, Rao CVS, Kennedy IR (2002) Facilitating a N -fixing Hayat R, Ali S, Ijaz SS, Chatha TH, Siddique MT (2008b) Estimation of symbiosis between diazotrophs and wheat. In: Kennedy IR, N -fixation of mung bean and mash bean through xylem uriede Choudhury ATMA (eds) Biofertilisers in action. Rural Industries technique under rainfed conditions. Pak J Bot 40(2):723–734 Research and Development Corporation, Canberra, pp 84–93 Hegazi NA, Faye M, Amin G, Hamza MA, Abbas M, Youssef H, Monib Jackson MB (1991) Ethylene in root growth and development. In: M (1998) Diazotrophs assoiciated with non-legumes grown in sandy Matoo AK, Suttle JC (eds) The plant hormone ethylene. CRC soil. In: Malik KA, Mirza MS, Ladha JK (eds) Nitrogen fixation Press, Boca Raton, pp 159–181 with non-legumes. Kulwer, Dordrecht, pp 209–222 Jadhav RS, Thaker NV, Desai A (1994) Involvement of the Herman MAB, Nault BA, Smart CD (2008) Effects of plant growth siderophore of cowpea Rhizobium in the iron nutrition of the promoting rhizobacteria on bell pepper production and green peanut. World J Microbiol Biotechnol 10:360–361 peach aphid infestation in New York. Crop Prot 27:996–1002 James EK, Reis VM, Olivares FL, Baldani JI, Döbereiner J (1994) Herridge DF, Marcellos H, Felton WL, Turner GL, Peoples MB Infection of sugar cane by the nitrogen-fixing bacterium (1993) Legume N fixation an efficient source of N for cereal Acetobacter diazotrophicus. J Exp Bot 45:757–766 production, Nuclear methods in soil-plant aspects of sustainable James EK, Gyaneshwar P, Barraquio WL, Mathan N, Ladha JK agriculture (Proc. Sem. Colombo, 1993). IAEA, Vienna (2000) Endophytic diazotrophs associated with rice. In: Ladha Hesselmann RPX, Werlen C, Hahn D, van der Meer JR, Zehnder AJB JK, Reddy PM (eds) The quest for nitrogen fixation in rice. (1999) Enrichment, phylogenetic analysis and detection of a International Rice Research Institute, Los Banõs, pp 119–140 bacterium that performs enhanced biological phosphate removal Jetiyanon K, Kloepper JW (2002) Mixtures of plant growth promoting in activated sludge. Syst Appl Microbiol 22:454–465 rhizobacteria for induction of systemic resistance against multiple Hilali A, Przrost D, Broughton WJ, Antoun A (2000) Potential use of plant diseases. Biol Control 24:285–291 Rhizobium leguminosarum by trifoli as plant growth promoting Joo GJ, Kin YM, Kim JT, Rhee IK, Kim JH, Lee IJ (2005) rhizobacteria with wheat. In: Abstract of the I7th North American Gibberellins producing rhizobacteria increase endogenous conference on symbiotic nitrogen fixation. Laval University, gibberellins content and promote growth of red peppers. J Quebec, Canada, pp 23-28 Microbiol 43(6):510–515 Hilali A, Prevost D, Broughton WJ, Anloun H (2001) Effects of in- Kajar B, Jensen J (1995) The inheritance of nitrogen and phosphorous oculation avec des souches de Rhizobium leguminosarum biovar content in barley analyzed by genetic markers. Heriditas trifolii sur la croissance du ble dans deux sols du Maroc. Can J 123:109–119 Microbiol 47:590–593 Kanungo PK, Panda D, Adhya TK, Ramakrishnan B, Rao VR (1997) Hoflich G (2000) Colonization and growth promotion of non-legumes Nitrogenase activity and nitrogen fixing bacteria associated with by Rhizobium bacteria. Micobial biosystems: new prontiers. In: rhizosphere of rice cultivars. J Sci Food Agric 73:485–488 594 Ann Microbiol (2010) 60:579–598 Keating JDH, Chapmanian N, Saxena MC (1998) Effect of improved suppression of Meloidogyne incognita on tomato (Lycopersicon management of legumes in a legume-cereal rotation on field esculentum). J Nematol 34:362–369 estimates of crop nitrogen uptake and symbiotic nitrogen fixation Kokalis-Burelle N, Vavrina CS, Rosskopf EN, Shelby RA (2002b) in northern Syria. J Agric Sci 110:651–659 Field evaluation of plant growth-promoting rhizobacteria amended transplant mixes and soil solarization for tomato and Kempster VN, Scott ES, Davies KA (2002) Evidance for systematic, pepper production in Florida. Plant Soil 238:257–266 cross-resistance in white clover (Trifolium repens) and annual medic (Medicago truncatula var truncatula) induced by biological Kokalis-Burelle N, Vavrina CS, Reddy MS, Kloepper JW (2003) and chemical agents. Biocontrol Sci Technol 12(5):615–623 Amendment of muskmelon and watermelon transplant media Kennedy IR, Tchan Y (1992) Biological nitrogen fixation in no with plant growth-promoting rhizobacteria: effects on disease and leguminous field crops: recent advances. Plant Soil 141:93–118 nematode resistance. Hortic Technol 13:476–482 Kennedy IR, Islam N (2001) The current and potential contribution of Kokalis-Burelle N, Kloepper JW, Reddy MS (2006) Plant growth- asymbiotic nitrogen requirements on farms: a review. Aust J Exp promoting rhizobacteria as transplant amendments and their Agric 41:447–457 effects on indigenous rhizosphere microorganisms. Appl Soil Kennedy IR, Pereg-Gerk LL, Wood C, Deaker R, Glichrist K, Ecol 31(1–2):91–100 Katupitiya S (1997) Biological nitrogen fixation in non- Kolb W, Martin P (1985) Response of plant roots to inoculation with leguminous field crops: facilitating the evolution of an Azospirillum brasilense and to application of indoleacetic acid. effective association between Azosirillun and wheat. Plant Soil In: Klingmüller W (ed) Azospirillum III: genetics, physiology, 194:65–79 ecology. Springer, Berlin, pp 215–221 Kennedy IR, Choudhury AIMA, KecSkes ML (2004) Non-Symbiotic Kumar V, Behl RK, Narula N (2001) Establishment of phosphate bacterial diazotrophs in crop-farming systems: can their potential solubilizing strains of Azotobacter chroococcum in the rhizosphere for plant growth promotion be better exploited? Soil Boil and their effect on wheat cultivars under greenhouse conditions. Biochem 3 6(8):1229-1244 Microbiol Res 156:87–93 Kerovuo J, Lauraeus M, Nurminen P, Kalkinen N, Apajalahti J (1998) Ladha JK, Reddy PM (2003) Nitrogen fixation in rice systems: state Isolation, characterization, molecular gene cloning, and sequencing of knowledge and future prospects. Plant Soil 252:151–167 of a novel phytase from Bacillus subtilis. Appl Environ Microbiol Ladha JK, Baraquio WL, Watanabe I (1982) Immunological techniques 64:2079–2085 to identify Azospirillum associated with rice. Can J Microbiol Khalid A, Arshad M, Zahir ZA (2001) Factor affecting auxin 28:478–485 biosynthesis by wheat and rice rhizobacteria. Pak J Soil Sci Lebuhn M, Heulin T, Hartmann A (1997) Production of auxin and other 21:11–18 indolic and phenolic compounds by Paenibacillus polymyxa strains Khalid A, Arshad M, Zahir ZA (2003) Growth and yield response of isolated from different proximity to plant roots. FEMS Microbiol wheat to inoculation with auxin producing plant growth Ecol 22:325–334 promoting rhizobacteria. Pak J Bot 35:483–498 Lee S, Pierson B, Kennedy C (2002) Genetics and biochemistry of Khalid A, Arshad M, Zahir ZA (2004) Screening plant growth- nitrogen fixation and other factors beneficial to host plant growth promoting rhizobacteria for improving groth and yield of wheat. in diazotrophic endophytes. In: Vanderleyden J (ed) Proceedings J Appl Microbiol 96:473–480 of the ninth international symposium on nitrogen fixation with Khan AG (2005) Role of soil microbes in the rhizosphere of plants nonlegumes. Katholique Universiteit, Leuven, pp 41–42 growing on trace metal contaminated soils in phytoremediation. J Leelahawonge C, Nuntagij A, Teaumroong N, Boonkerd N, Pongsilp N Trace Elem Med Biol 18:355–364 (2010) Characterization of root-nodule bacteria isolated from the Kim YO, Lee JK, Kim HK, Yu JH, Oh TK (1998) Cloning of the medicinal legume Indigofera tinctoria. Ann Microbiol 60:65–74 thermo stable phytase gene (phy) from Bacillus sp. DS11 and its Lhuissier FGP, de Ruijter NCA, Sieberer BJ, Esseling JJ, Emons over expression in Escherichia coli. FEMS Microbiol Lett AMC (2001) Time course of cell biological events evoked in 162:185–191 legume root hairs by Rhizobium Nod factors: state of the art. Ann Klee HJ, Hayford MB, Kretzmer KA, Barry GF, Kishore GM (1991) Bot 87:289–302 Control of ethylene synthesis by expression of a bacterial enzyme Li J, Ovakin DH, Charles TC, Glick BR (2000) An ACC deaminase in transgenic tomato plants. Plant Cell 3:1187–1193 minus mutatnt of Entreobacter cloacae UW4 no longer promotes Kloepper JW (1993) Plant growth promoting rhizobacteria as root elongation. Curr Microbiol 41:101–105 biological control agents. In: Metting FB Jr (ed) Soil microbial Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R ecology. Dekker, New York, pp 255–274 (2003) LysM domain receptor kinase regulating rhizobial nod Kloepper JW (1994) Plant growth promoting rhizobacteria. In: Okon factor-induced infection. Science 302:630–633 Y (ed) Azospirillum/Plant associations. CRC Press, Boca Raton, Loper JE, Buyer JS (1991) Siderophores in microbial interactions on pp 137–166 plant surfaces. Mol Plant Microb Interact 4:5–13 Kloepper JW, Schroth MN (1978) Plant growth promoting rhizobacteria Lucas GJA, Probanza A, Ramos B, Colon Flores JJ, Gutierrez Mañero on radishes. Proceedings of the Fourth International Conference on FJ (2004a) Effect of plant growth promoting rhizobacteria Plant Pathogen Bacteria, vol. 2. INRA, pp 879–882 (PGPRs) on biological nitrogen fixation, nodulation and growth Kloepper JW, Beauchamp CJ (1992) A review of issues related to of Lupinus albus I. cv. Multolupa. Eng Life Sci 7:1–77 measuring colonization of plant roots by bacteria. Can J Microbiol Lucas GJA, Probanza A, Ramos B, Palomino MR, Gutierrez Mañero 38:1219–1232 FJ (2004b) Effect of inoculation of Bacillus licheniformis on Kloepper JW, Lifshitz R, Zablotowicz RM (1989) Free-living bacterial tomato and pepper. Agronomie 24:169–176 inocula for enhancing crop productivity. Trends Biotechnol 7:39–43 Lupwayi NZ, Rice WA, Clayton GW (2000) Endophytic Rhizobia in Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance barley and canola in rotation with field peas. In: Book of and promotion of plant growth by Bacillus spp. Phytopathology abstracts, 17th North American conference on symbiotic nitrogen 94(11):1259–1266 fixation, 23-28 July 2000, 80. University of Laval, Quebec, Kokalis-Burelle N (2003) Effects of transplant type and soil fumigant on Canada, p 51 growth and yield of strawberry in Florida. Plant Soil 256:273–280 Lynch JM (1983) Soil biotechnology. Blackwell, Oxford Kokalis-Burelle N, Martinez-Ochoa N, Rodríguez-Kábana R, Kloepper Lynch JM (1990) Beneficial interactions between miroorganisms and JW (2002a) Development of multi-component transplant mixes for roots. Biotechnol Adv 8:335–346 Ann Microbiol (2010) 60:579–598 595 Malik KA, Mirza MS, Hassan U, Mehnaz S, Rasul G, Haurat J, Bauy Narasimhan K, Basheer C, Bajic VB, Swarup S (2003) Enhancement of R, Normanel P (2002) The role of plant associated beneficial plant-microbe interactions using a rhizosphere metabolomics-driven bacteria in rice-wheat Cropping System. In: Kennedy IR, approach and its application in the removal of polychlorinated Chaudhry ATMA (eds) Biofertilisers in action. Rural industries biphenyls. Plant Physiol 132:146–153 research and development Corporation, Canberra, pp 73–83 Nautiyal CS, Bhadauria S, Kumar P, Lal H, Mondal R, Verma D Mantelin S, Touraine B (2004) Plant growth-promoting bacteria and (2000) Stress induced phosphate solubilization in bacteria nitrate availability: impacts on root development and nitrate isolated from alkaline soils. FEMS Microbiol Lett 182:291–296 uptake. J Exp Bot 55:27–34 Nieto KF, Frankenberger WT Jr (1990a) Influence of adenine, Martinez-Romero E, Gutierrez-Zamora ML, Estrada P, Caballero- isopentyl alcohol and Azotobacter chroococcum on the growth Mellado J, Hernandez-Lucas I (2000) Natural endophytic associa- of Raphanus sativus. Plant Soil 127:147–156 tion between Rhizobium Etli and maize. In: Book of abstracts, 17th Nieto KF, Frankenberger WT Jr (1990b) Microbial production of North American conference on symbiotic nitrogen fixation, 23-28 cytokinins. In: Bollag JM, Stotzky G (eds) Soil biochem, vol 6. July 2000. University of Laval, Quebec, Canada, p 51 Dekker, New York, pp 191–248 Martinez-Toledo MV, Rodelas B, Salmeron V, Pozo C, Gonzalez- Nieto KF, Frankenberger WT Jr (1991) Influence of adenine, isopentyl Lopez J (1996) Production of pantothenic acid and thiamine by alcohol and Azotobacter chroococcum on the vegetative growth Azotobacter vinelandii in a chemically defined medium and a of Zea mays. Plant Soil 135:213–221 dialysed soil medium. Biol Fertil Soils 22:131–135 Noling JW, Gilreath JP (2001) Methyl bromide, progress and Matiru VN, Dakora FD (2004) Potential use of rhizobial bacteria as problems: identifying alternatives to methyl bromide, vol. II. promoters of plant growth for increased yield in landraces of Citrus and Veg. Mag., IFAS, University of Florida African cereal crops. Afr J Biotechnol 3(1):1–7 O´Sullivan DJ, O´Gara F (1992) Traits of fluorescent Pseudomonas McGrathJW, Wisdom GB,McMullanG,Lrakin MJ, QuinnJP spp. involved in suppression of plant root pathogens. Microbiol (1995) The purification and properties of phosphonoacetate Rev 56:662–676 hydrolase, a novel carbon-phosphorus bond-cleaving enzyme Ohr HD, Sims JJ, Grech NM, Becker JO, McGiffen ME Jr (1996) from Pseudomonas fluorescens 23F. Eur J Biochem 234:225– Methyl iodide, an ozone-safe alternative to methyl bromide as a soil fumigant. Plant Dis 80:27–32 McGrath JW, Hammerschmidt F, Quinn JP (1998) Biodegradation of Ohtake H, Wu H, Imazu K, Ambe Y, Kato J, Kuroda A (1996) phosphonomycin by Rhizobium huakuii PMY1. Appl Environ Bacterial phosphonate degradation, phosphite oxidation and Microbiol 64:356–358 polyphosphate accumulation. Res Conserv Recycl 18:125–134 Mclnroy JA, Kloepper JW (1995) Survey of indigenous endophytes Okon Y, Labandera-Gonzalez CA (1994) Agronomic applications of from cotton and sweet corn. Plant Soil 173:337–342 Azospirillum: an evaluation of 20 years world-wide field Meyer SLF, Massoud SI, Chitwood DJ, Roberts DP (2000) Evaluation inoculation. Soil Biol Biochem 26:1591–1601 of Trichoderma virens and Burkholderia cepacia for antagonistic Okon Y, Itzigsohn R (1995) The development of Azospirillum as a activity against root-knot nematode, Meloidogyne incognita. commercial innoculant for improving crop yields. Biotechnol Nematology 2:871–879 Adv 13(3):415–424 Middledrop PJM, Briglia M, Salkinoja-Salonen M (1990) Biodeg- Pal KK, Tilak KVBR, Saxena AK, Dey R, Singh CS (2001) radation of pentachlorophenol in natural polluted soil by Suppression of maize root diseases caused by Macrophomina inoculated Rhodococcus chlorophenolicus.MicrobEcol phaseolina, Fusarium moniliforme and Fusarium germinearum 20:123–139 by plant growth promoting rhizobacteria. Microbiol Res Miller RM, Jastrow JD (2000) Mycorrhizal fungi influence soil 156:209–223 structure. In: Kapulnik Y, David DD, David DD Jr (eds) Pandey A, Kumar S (1989) Potential of Azotobacters and Azospirilla Arbuscular mycorrhizas: physiology and function. Springer, as biofertilizers for upland agriculture: a review. J Sci Ind Res Berlin 48:134–144 Milton HSJ (2007) Beneficial bacteria and bioremediation. Water Air Panwar JDS, Singh O (2000) Response of Azospirillum and Bacillus Soil Pollut 184:1–3 on growth and yield of wheat under field conditions. Indian J Mirza MS, Rasul G, Mehnaz S, Ladha JK, So RB, Ali S, Malik KA Plant Physiol 5:108–110 (2000) Beneficial effects of inoculated nitrogen-fixing bacteria on Park KS, Kloepper JW (2000) Activation of PR-1a promoter by rice. In: Ladha JK, Reddy PM (eds) The quest for nitrogen rhizobacteria which induces systemic resistance in tobacco fixation in rice. International Rice Research Institute, Los Banõs, against Pseudomonas syringae pv. Tabaco Biol Cont 18:2–9 pp 191–204 Patil PL, Patil SP (1984) Uptake of nitrogen by cotton inoculated with Muratova A Yu, Turkovskaya OV, Antonyuk LP, Makarov OE, Azotobacter. J Maharashtra Agric Uni 9(17):1–172 Pozdnyakova LI, Ignatov VV (2005) Oil-oxidizing potential of Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic associative rhizobacteria of the genus Azospirillum. Microbiology acid. Can J Microbiol 42:207–220 74:210–215 Patten CL, Glick BR (2002) Role of Pseudomonas putida indole-acetic Murphy JF, Zender GW, Schuster DJ, Sikora EJ, Polston JE, Kloepper acid in development of the host plant root system. Appl Environ JW (2000) Plant growth promoting rhizobacterial mediated Microbiol 68:3795–3801 protection in tomato against tomato mottle virus. Plant Dis Paynel F, Murray PJ, Cliquet B (2001) Root exudates: a pathway for 84:779–784 short-term N transfer from clover and ryegrass. Plant Soil Murray JD, Bogumil JK, Shusei SH, Satoshi T, Lisa A, Krzysztof S 229:235–243 (2007) A cytokinin perception mutant colonized by Rhizobium in Peix A, Rivas-Boyero AA, Mateos PF, Rodriguez-Barrueco C, the absence of nodule organogenesis. Science 315(5808):101–104 Martínez-Molina E, Velazquez E (2001) Growth promotion of Muthukumarasamy R, Revathi G, Lakshminarasimhan C (1999) chickpea and barley by a phosphate solubilizing strain of Diazotrophic associations in sugar cane cultivation in South Mesorhizobium mediterraneum under growth. Soil Biol Biochem India. Trop Agric 76:171–178 33:103–110 Nakata PA (2002) The generation of a transposon-mutagenized Pereira JAR, Cavalcante VA, Baldani JI, Döbereiner J (1988) Field Burkholderia glumae library to isolate novel mutants. Plant Sci inoculation of sorghum and rice with Azospirillum sp and 162:267–271 Herbaspirillum seropedicae. Plant Soil 110:269–274 596 Ann Microbiol (2010) 60:579–598 Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the Roesti D, Guar R, Johri BN, Imfeld G, Sharma S, Kawaljeet K, Aragno M underground: molecular plant-rhizobacteria interactions. Plant (2006) Plant growth stage, fertilizer management and bio- Cell Environ 26:189–199 inoculation of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria affect the rhizobacterial community Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, structure in rain-fed wheat field. Soil Biol Biochem 38:1111–1120 Machado De Oliveira R, Leid M, McBurney MW, Guarente L (2004) Sirt1 promotes fat mobilization in white adipocytes by Roper MM, Ladha JK (1995) Biological N -fixation by heterotrophic repressing PPAR-gamma. Nature 429(77):1–776 and phototrophic bacteria in association with straw. Plant Soil Plessner O, Klapach T, Guerinot ML (1993) Siderophore utilization by 174:211–224 Bradyrhizobium japonicum. Appl Environ Microbiol 59:1688– Rossolini GM, Shipa S, Riccio ML, Berlutti F, Macaskie LE, Thaller 1690 MC (1998) Bacterial non-specific acid phosphatases: physiology, evolution, and use as tools in microbial biotechnology. Cell Mol Primrose SB (1979) Ethylene and agriculture: the role of the microbe. Life Sci 54:833–850 J Appl Bacteriol 46:1–25 Raj SN, Deepak SA, Basavaraju P, Shetty HS, Reddy MS, Kloepper JW Russo A, Vettori L, Felici C, Fiaschi G, Morini S, Toffanin A (2008) Enhanced cropropagation response and biocontrol effect of (2003) Comparative performance of formulations of plant growth Azospirillum brasilense Sp245 on Prunus cerasifera L. clone promoting rhizobacteria in growth promotion and suppression of Mr.S 2/5 plants. J Biotechnol 134(3–4):312–319 downy mildew in pearl millet. Crop Prot 22:579–588 Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW Rao DLN (2001) BNF research progress 1996-2000: all India (2004) Bacterial volatiles induce systemic resistance in Arabi- coordinated research project on biological nitrogen fixation. dopsis. Plant Physiol 134:1017–1026 IISS, Bhopal Ryu CM, Kim J, Choi O, Kim SH, Park CS (2006) Improvement of Reid M (1987) Ethylene in plant growth, development and biological control capacity of Paenibacillus polymyxa E681 by senescence. In: Davies PJ (ed) Plant hormones and their role seed pelleting on sesame. Biol Control 39:282–289 in plant growth and development. Martinus Nijhoff, Boston, Şahin F, Çakmakçi R, Kantar F (2004) Sugar beet and barley yields in pp 257–279 relation to inoculation with N -fixing and phosphate solubilizing Reilly TJ, Baron GS, Nano F, Kuhlenschmidt MS (1996) bacteria. Plant Soil 265:123–129 Characterization and sequencing of a respiratory burst Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of inhibiting acid phosphatase from Francisella tularensis.JBiol Chem 271:10973–10983 plant growth promoting rhizobacteria (PGPR) containing ACC Reinhold-Hurek B, Hurek T, Gillis M, Hoste B, Vancanneyt M, deaminase in stress agriculture. J Ind Microbiol Biotechnol Kersters K, DeLey J (1993) Azoarcus gen. nov., nitrogen fixing 34:635–648 proteobacteria associated with roots of Kallar grass (Leptochloa Saleh S, Huang XD, Greenberg BM, Glick BR (2004) Phytoremedia- fusca (L.) Kunth) and description of two species, Azoarcus tion of persistent organic contaminants in the environment. In: indigens sp. nov. and Azoarcus communis sp. nov. Int J Syst Singh A, Ward O (eds) Soil biology, vol. 1. Applied bioreme- Bacteriol 43:574–584 diation and phytoremediation. Springer, Berlin, pp 115–134 Reinhold-Hurek B, Egener T, Hurek T, Martin D, Sarkar A, Zhang L, Saravanakumar D, Lavanya N, Muthumeena B, Raguchander T, Miche L (2002) Regulation of nitrogen fixation and assimilation Suresh S, Samiyappan R (2008) Pseudomonas fluorescens of Azoarcus sp. BH72 new approaches to study biodiversity of enhances resistance and natural enemy population in rice plants grass endophytes. In: Vanderleyden J (ed) Proceedings of the against leaf folder pest. J Appl Entomol 132(6):469–479 nineth international symposium on nitrogen fixation with non- Sasikala C, Ramana CV (1995) Biotechnological potentials of legumes. Katholique Universideit Leuven, Belgium, p 48 anoxygenic phototrophic bacteria. I. Production of single-cell Reis VM, Baldani JI, Baldani VLD, Döberener J (2000) Biological protein, vitamins, ubiquinones, hormones, and enzymes and use in waste treatment. Adv Appl Microbiol 41:173–226 dinitrogen fixation in the graminae and palm trees. Crit Rev Plant Saubidet MI, Fatta N, Barneix AJ (2000) The effects of inoculation Sci 19:227–247 with Azospirillum brasilense on growth and nitrogen utilization Revillas JJ, Rodelas B, Pozo C, Martinez-Toledo MV, Gonzalez LJ by wheat plants. Plant Soil 245(2):15–222 (2000) Production of B-group vitamins by two Azotobacter Schippers B, Bakker AW, Baker PAHM (1987) Interactions of strains with phenolic compounds as sole carbon source under deleterious and beneficial rhizosphere microorganisms and the diazotrophic and adiazotrophic conditions. J Appl Microbiol effect of cropping practices. Annu Rev Phytopathol 25:339–358 89:486–493 Schippers B, Scheffer RJ, Lugtenberg JJ, Weisbek PJ (1995) Richardson AE (2001) Prospects for using soil microorganisms to Biocoating of seed with plant growth promoting rhizobacteria improve the acquisition of phosphorus by plants. Aust J Plant to improve plant establishment. Outlook Agric 24:179–185 Physiol 28:897–906 Schloter M, Wiehe W, Assmus B, Steindl H, Becke H, Hoflich G, Richardson AE, Hadobas PA (1997) Soil isolates of Pseudomonas Hartman A (1997) Root colonization of different plants by plant spp. that utilize inositol phosphates. Can J Microbiol 43(509– growth-promoting Rhizobium leguminosarum bv trifolii R39 5):16 Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their studied with monospecific polyclonal antisera. Appl Environ role in plant growth promotion. Biotechnol Adv 17:319–339 Microbiol 63:2038–2046 Rodríguez H, Han Y, Lei XG (1999) Cloning, sequencing and Séguin A, Lalonde M (1989) Detection of pectolytic activity and pel expression of an Escherichia. coli acid phopshatase/phytase gene homologous sequences in Frankia. Plant Soil 118:221–229 (app A2) isolated from pig colon. Biochem Biophys Res Serrano A, Mateos MI, Losada M (1993) Differential regulation by Commun 257:117–123 trophic conditions of phosphorylating and nonphosphorylating Rodríguez H, Rossolini GM, Gonzalez T, Jiping L, Glick BR (2000) NADP(+)-dependent glyceraldehyde-3-phosphate dehydro- Isolation of a gene from Burkholderia cepacia IS-16 encoding a genases in Chlorella fusca. Biochem Biophys Res Commun protein that facilitates phosphatase activity. Curr Microbiol 193:1348–1356 40:362–366 Shah Z, Shah SH, Peoples MB, Schwenke GD, Hrridge DF (2003) Rodríguez H, Fraga R, Gonzalez T, Bashan T (2006) Genetics of Crop residue and fiertilizer N effects on nitrogen fixation and phosphate solubilization and its potential applications for improving yields of legume-cereal rotations and soil organic fetility. Field plant growth-promoting bacteria. Plant Soil 287:15–21 Crops Res 83:1–11 Ann Microbiol (2010) 60:579–598 597 Shaharoona B, Arshad M, Zahir ZA (2006a) Effect of plant growth Thaller MC, Berlutti F, Schippa S, Lombardi G, Rossolini GM promoting rhizobacteria containing ACC-deaminase on maize (Zea (1994) Characterization and sequence of PhoC, the principal mays L.) growth under axenic conditions and on nodulation in phosphate-irrepressible acid phosphatase of Morganella mung bean (Vigna radiata L.). Lett Appl Microbiol 42:155–159 morganii. Microbiology 140:1341–1350 Shaharoona B, Arshad M, Zahir ZA, Khalid A (2006b) Performance Thaller MC, Berlutti F, Schippa S, Iori P, Passariello C, Rossolini GM of Pseudomonas spp. containing ACC-deaminase for improving (1995a) Heterogeneous patterns of acid phosphatases containing growth and yield of maize (Zea mays L.) in the presence of low-molecular-mass Polipeptides in members of the family nitrogenous fertilizer. Soil Biol Biochem 38:2971–2975 Enterobacteriaceae. Int J Syst Bacteriol 4:255–261 Shankariah C, Hunsigi G (2001) Field responses of sugarcane to Thaller MC, Lombardi G, Berlutti F, Schippa S, Rossolini GM (1995b) associative N fixers and P solubilishers. In: Hogarth DM (ed) Cloning and characterization of the NapA acid phosphatase/ Proceedings of the 24th international society of sugarcane phosphotransferase of Morganella morganii: identification of a Technologists Congress, 17-21 September 2001. The Australian new family of bacterial acid phosphatase encoding genes. Society of Sugercane Technologists, Brisbane, pp 40–45 Microbiology 140:147–151 Shenoy VV, Kalagudi GM (2005) Enhancing plant phosphorus use Tien TM, Diem HG, Gaskins MH, Hubbell DH (1981) Polygaracturonic efficiency for sustainable cropping. Biotechnol adv 23:501–513 acid transeliminase production by Azospirillum species. Can J Shiferaw B, Bantilan MCS, Serraj R (2004) Harnessing the potential Microbiol 27:426–431 of BNF for poor farmers: technological policy and institutional Tisdale SL, Nelson WL, Beaton JD (1990) Soil fertility and fertilizers, constraints and research need. In: Serraj R (ed) Symbiotic 4th edn. Macmillan, New York nitrogen fixation; prospects for enhanced application in tropical Tran Vân V, Berge O, Ke SN, Balandreau J, Heulin T (2000) Repeated agriculture. Oxford & IBH, New Delhi, p 3 beneficial effects of rice inoculation with a strain of Burkholderia Shoebitz M, Ribaudo CM, Pardo MA, Cantore ML, Ciampi L, Curá vietnamiensis on early and late yield components in low fertility JA (2009) Plant growth promoting properties of a strain of sulphate acid soils of Vietnam. Plant Soil 218:273–284 Enterobacter ludwigii isolated from Lolium perenne rhizosphere. Tye AJ, Siu FK, Leung TY, Lim BL (2002) Molecular cloning and the Soil Biol Biochem 41(9):1768–1774 biochemical characterization of two novel phytases from Bacillus Siddiqui IA, Ehteshamul-Haque S, Shaukat SS (2001) Use of subtilis 168 and Bacillus licheniformis. Appl Microbiol Biotechnol rhizobacteria in the control of root rot-root knot disease complex 59:190–197 of mung bean. J Phytopathol 149:337–346 Umali-Garcia M, Hubbell DH, Gaskins MH, Dazzo FB (1980) Sierra S, Rodelas B, Martinez-Toledo MV, Pozo C, Gonzalez-Lopez J Association of Azospirillum with grass roots. Appl Environ (1999) Production of B-group vitamins by two Rhizobium strains Microbiol 39(1):219–226 in chemically defined media. J Appl Microbiol 86:851–858 Valverde F, Losada M, Serrano A (1999) Engineering a central Skrary FA, Cameron DC (1998) Purification and characterization of a metabolic pathway: glycolysis with no net phosphorylation in an Bacillus licheniformis phosphatase specific for D-alpha- Escherichia coli gap mutant complemented with a plant Gap N glycerphosphate. Arch Biochem Biophys 349:27–35 gene. FEBS Lett 449:153–158 Snapp SS, Aggarwal VD, Chirwa RM (1998) Note on phosphorus and van Loon LC, Bakker P, Pieterse CMJ (1998) Systemic resistance induced genotype enhancement of biological nitrogen fixation and productiv- by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483 ity of maize/bean intercrops in Malawi. Field Crops Res 58:205–212 Van Rhijn P, Fujishige NA, Lim PO, Hirsch AM (2001) Sugar-binding Soliman S, Seeda MA, Aly SSM, Gadalla AM (1995) Nitrogen activity of pea lectin enhances heterologous infection of fixation by wheat plants as affected by nitrogen fertilizer levels transgenic alfalfa plants by Rhizobium leguminosarum bivor and nonsymbiotic bacteria. Egypt J Soil Sci 35:401–413 viciae. Plant Physiol 126:133–144 Spencer D, James EK, Ellis GJ, Shaw JE, Sprent JI (1994) Interactions Van Veen JA, van Overbeek LS, van Elsas JD (1997) Fate and activity between Rhizobia and potato tissue. J Exp Bot 45:1475–1482 of microorganisms introduced into soil. Microbiol Mol Biol Rev Stajner D, Gasaić O, Matković B, Varga SZI (1995) Metolachlor 61:121–135 effect on antioxidants enzyme activities and pigments content in Vandamme P, Goris J, Chen WM, de Vos P, Willems A (2002) seeds and young leaves of wheat (Triticum aestivum L.). Agr Burkholderia tuberum sp. nov and Burkholderia phymatum sp. Med 125:267–273 nov., nodulate the roots of tropical legumes. Syst Appl Microbiol Stajner D, Kevreaan S, Gasaić O, Mimica-Dudić N, Zongli H (1997) 25:507–512 Nitrogen and Azotobacter chroococcum enhance oxidative stress Venkateswarlu B, Hari K, Katyl JC (1997) Influence of soil and crop tolerance in sugar beet. Biol Plant 39:441–445 factors on the native rhizobia populations in soils under dry land Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living farming. Appl Soil Ecol 7:1–10 nitrogen-fixing bacterium closely associated with grasses: genetic, Vestberg M, Kukkonen S, Saari K, Parikka P, Huttunen J, Tainino L, biochemical and ecological aspects. FEMS Microbiol Rev Devos N, Weekers F, Kevers C, Thonart P, Lemoine MC, Cordier C, 24:487–506 Alabouvette C, Gianinazzi S (2004) Microbial inoculation for Stout MJ, Zehnder GW, Baur ME (2002) Potential for the use of improving the growth and health of micropropagated strawberry. elicitors of plant defence in arthropode management programs. Appl Soil Ecol 27:243–258 Arch Insect Biochem Physiol 51(4):222–235 Vivas A, Barea JM, Azcón R (2005) Brevibacillus brevis isolated from Sturz AV, Christie BR, Novak J (2000) Bacterial endophytes: potential cadmium- or zinc-contaminated soils improves in vitro spore role in developing sustainable system of crop production. Crit germination and growth of Glomus mosseae under high Cd or Zn Rev Plant Sci 19:1–30 Concentrations. Microb Ecol 49:416–442 Sutton JC, Peng G (1993) Biocontrol of Botrytis cinerea in strawberry Wachowska U, Majchrzak B, Borawska M, Karpinska Z (2004) leaves. Phytopathology 83:615–621 Biological control of winter wheat pathogens by bacteria. Acta Terouchi N, Syono K (1990) Rhizobium attachment and curling in fytotech zootech, Vol. 7, 2004, Special Number, Proceedings of asparagus, rice, and oat plants. Plant Cell Physiol 31:119–127 the XVI. Slovak and Czech Plant Protection Conference Thakuria D, Taleekdar NC, Goswami C, Hazarika S, Boro RC, Khan organized at Slovak Agricultural University in Nitra, Slovakia MR (2004) Characterization and screening of bacteria from Walsh UF, Morrissey JP, O’Gara F (2001) Pseudomonas for biocontrol rhizosphere of rice grown in acidic soils of Assam. Curr Sci 86 of phytopathogens: from functional genomics to commercial (7):978–985 exploitation. Curr Opin Biotechnol 12:289–295 598 Ann Microbiol (2010) 60:579–598 Webster G, Gough C, Vasse J, Batchelor CA, O’Callaghan KJ, nodulation of lentil (Lens culinaris Medic) seedlings under Kothari SL, Davey MR, Denarie J, Cocking EC (1997) axenic conditions. Soil Environ 26(1):81–91 Interactions of Rhizobia with rice and wheat. Plant Soil Zahir AZ, Arshad M, Frankenberger WT Jr (2004) Plant growth 194:115–122 promoting rhizobacteria: application and perspectives in Agriculture. Adv Agron 81:97–168 Wiehe W, Holfich G (1995) Survival of plant growth promoting Zahir ZA, Abbas SA, Khalid M, Arshad M (2000) Substrate rhizosphere bacteria in rhizosphere of different crops and dependent microbially derived plant hormones for improving migration to non-inoculated plants under field conditions in growth of maize seedlings. Pak J Biol Sci 3:289–291 north-east Germany. Microbiol Res 150:201–206 Zaidi S, Usmani S, Singh BR, Musarrat J (2008) Significance of Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation Bacillus subtilis strains SJ-101 as a bioinoculant for concurrent in higher plants. Annu Rev Plant Physiol 35:155–189 plant growth promotion and nickel accumulation in Brassica Yanni YG, El-Fattah FKA (1999) Towards integrated biofertiliza- Juncea. Chemosphere 64:991–997 tion management with free living and associative dinitrogen fixers for enhancing rice performance in the Nile delta. Zavalin AA, Kandaurova TM, Vinogradova LV (1998) Influence of Symbiosis 27:319–331 nitrogen fixing microorganisms on the nutrition and productivity Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip- of spring wheat, and on the characteristics of photosynthesis of Hollingsworth S, Orgambide G, de Bruijn F, Stoltzfus J, Buckley different varieties of spring wheat. In: Elmerich C, Kondorosi A, D, Schmidt TM, Mateos PF, Ladha JK, Dazzo FB (1997) Natural Newton WE (eds) Biological nitrogen fixation for the 21st endophytic association between Rhizobium leguminosarum bv. century. Kluwer, Dordrecht, pp 413–414 trifolii and rice roots and assessment of its potential to promote Zhang S, Moyne AL, Reddy MS, Kloepp JW (2002) The role of rice growth. Plant Soil 194:99–114 salicylic acid in induced systemic resistance elicited by plant Yanni YG, Rizk RY, Abd El-Fattah FK, Squartini A, Corich V, growth-promoting rhizobacteria against blue mold of tobacco. Giacomini A, de Bruijn F, Rademaker J, Maya-Flores J, Biol Control 25:288–296 Ostrom P, Vega-Hernandez M, Hollingsworth RI, Martinez- Zhang H, Sekiguchi Y, Hanada S, Hugenholtz P, Kim H, Kamagata Y, Molina E, Ninke K, Philip-Hollingsworth S, Mateos PF, Nakamura K (2003) Gemmatimonas aurantiaca gen. nov., sp. nov., Velasquez E, Triplett E, Umali-Garcia M, Anarna JA, Rolfe a Gram-negative, aerobic, polyphosphate accumulating micro- BG, Ladha JK, Hill J, Mujoo R, Ng PK, Dazzo FB (2001) organism, the first cultured representative of the new bacterial The beneficial plant growth-promoting association of Rhizo- phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol 53:1155–1163 bium leguminosarum bv. trifolii with rice roots. Aust J Plant Zhuang XL, Chen J, Shim H, Bai Z (2007) New advances in plant Physiol 28:845–870 growth-promoting rhizobacteria for bioremediation. Environ Int Zafar-ul-Hye M, Zahir ZA, Shahzad SM, Irshad U, Arshad M (2007) 33:406–413 Isolation and screening of Rhizobia for improving growth and

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Annals of Microbiology – Springer Journals

Published: Aug 28, 2010

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