Access the full text.
Sign up today, get DeepDyve free for 14 days.
Botrytis cinerea is a significant necrotrophic plant pathogen causing devastating diseases on more than 500 plant species, especially on fresh fruits and vegetables, resulting in the economic losses ranging from $10 billion to $100 billion worldwide. This fungal pathogen invades nearly all parts of plants including stems, leaves, flowers, fruits, and seeds at both pre-harvest and post-harvest stages. Due to its wide host range and the huge economic losses that it causes, extensive investigations have been carried out to effectively control this plant pathogen. It is beneficial for exploring the pathogenic mechanisms of B. cinerea to provide fundamental basis for control strategies. In recent years, tremendous progress has been made in understanding these pathogenic genes and regulatory pathways, as well as the control strategies of B. cinerea. Here, the current knowledge will be summarized in this review. Key words: gray mould rot; horticultural crops; pathogenesis; control technology. because it has broad host range, various attack modes, and both Introduction asexual and sexual stages to survive in favourable or unfavour- Botrytis cinerea is one of the most extensively studied necrotrophic able conditions (Fillinger and Elad, 2016). The asexual spores of fungal pathogens and causes gray mold rot in more than 500 plant B. cinerea are conidia, which are easily to be dispersed by wind or species (Williamson et al., 2007). This pathogen has a disastrous eco- water, and the sexual spores of B. cinerea are sclerotia, which are nomic impact on various economically important crops including essential for survival under adverse environment (Brandhoff et al., grape, strawberry, and tomato (Dean et al., 2012) and is able to be 2017). To date, the principal means to control grey mold rot caused present inside stems, leaves, flowers, fruits, and seeds. It may trigger by B. cinerea remain as the application of synthetic fungicides, which obvious disease symptoms in the pre-harvest period or remain qui- may be about 8 percent of all the global fungicide market, and the escent until post-harvest period (Fillinger and Elad, 2016). Botrytis annual global expenses at Botrytis control usually exceed €1 billion cinerea has been reckoned as one of the most important post-har- (Dean et al., 2012). However, the control effects of fungicides are vest pathogens in fresh fruits and vegetables (Zhang et al., 2014a). not satisfactory on B. cinerea whose genome is plasticity and prone The annual economic losses of B. cinerea easily exceed $10 billion to develop drug resistance genes. In addition, fungicides are not safe worldwide (Weiberg et al., 2013). Due to its scientific and economic for human and environment (Droby et al., 2009). Therefore, it is importance, B. cinerea has been classified as the second important important to deeply understand the molecular basis of pathogenesis plant pathogen (Dean et al., 2012). It is difficult to control B. cinerea © The Author(s) 2018. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/ by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact firstname.lastname@example.org Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/111/5057759 by Ed 'DeepDyve' Gillespie user on 28 August 2018 112 L. Hua et al. 2018, Vol. 2, No. 3 of B. cinerea and develop new strategies to prevent grey mold rot As signalling molecules, it is necessary for ROS to move from caused by B. cinerea in fresh fruits. In recent years, great efforts have the place of origin to the site of action. The transformation mol- been put on exploring the molecular mechanisms of B. cinerea, since ecules of ROS are obscure since ROS are composed of various highly its genome information (strain B05.10) is available (Amselem et al., reactive molecules including radicals (.O2 and .OH) and molecules 2011), and the functions of various genes especially those pathogen- (H O and O ), which are difficult to investigate. Among the ROS 2 2 3 esis-related proteins are unravelled. molecules, H O is stable and suitable for investigation (Waghray 2 2 In this review, we mainly introduce the latest information about et al., 2005). H O can function as both intracellular and intercellu- 2 2 molecular pathogenesis of B. cinerea, which is beneficial for under - lar signal molecules (Pletjushkina et al., 2006; Rice, 2011). However, standing the theoretical knowledge about molecular pathogenic H O is unable to cross the membrane lipid bilayer freely by sim- 2 2 mechanisms of the fungal pathogen, as well as current control strat- ple diffusion, it needs to the aid of membrane lipid compositions egies against gray mould rot in fresh fruits. or channel proteins to cross over plasma membranes (Seaver and Imlay, 2001). Aquaporins, which are known as efficient water chan- nels, have been demonstrated to mediate the transportation of H O 2 2 across membranes (Bienert et al., 2007; Miller et al., 2010). Our Pathogenic Mechanisms of B. cinerea studies indicated that aquaporin8 (BcAQP8) in B. cinerea could play Roles of reactive oxygen species in pathogenesis a crucial role in the transmembrane transportation of ROS, and the Reactive oxygen species (ROS) are a collective of highly react- distribution of mitochondria, which is the main source of ROS (An 2− ive molecules including superoxide anion (.O ), hydroxyl radical et al., 2016). Besides to regulate ROS transportation, BcAQP8 also (.OH), and certain non-radical oxidizing agents such as hydrogen affects the expression of BcNoxR, the regulatory subunit of NOX. peroxide (H O ) and ozone (O ) that can be converted into radicals. 2 2 3 Deletion of bcaqp8 results in decrease in growth, sporulation, and ROS have an ambivalent role since they damage DNA, causing lipid pathogenicity of B. cinerea (An et al., 2016) (Figure 1). peroxidation and protein oxidation (Heller and Tudzynski, 2011; Qin et al., 2011), but also function as diffusible second messengers Roles of extracellular proteins in pathogenesis (Orozco-Cárdenas et al., 2001; Heller and Tudzynski, 2011). In the Plant cell wall is among the first lines of defence that an invasive early stage of infection, plant hosts usually trigger oxidative burst pathogen encounters. They are heterogeneous structures mainly which generate large amounts of ROS transiently to counteract the composed of polysaccharides and proteins (Kubicek et al., 2014). invasive pathogen (Mellersh et al., 2002; Tian et al., 2013). However, As a necrotrophic fungus, the appressorium of B. cinerea was not as a necrotrophic fungus, B. cinerea can exploit the oxidative burst strong enough to breach the plant cell wall (Choquer et al., 2007). and even contribute to it by producing its own ROS. Therefore, it is necessary for B. cinerea to secrete a series of cell wall– ROS can be generated in B. cinerea either as unavoidable byprod- degrading enzymes (CWDEs) to degrade the structural polysaccha- ucts of metabolic processes or as the major products of NADPH rides of the host cell wall. In B. cinerea, 1155 genes are predicted oxidase (NOX) (Li et al., 2016). NOX is a multi-subunit complex to encode enzymes to degrade, modify, or create glycosidic bonds. which reduces oxygen to superoxide with the electron supplied by Among them, 275 have signal peptide sequence indicating their func- NADPH (Bedard et al., 2007). The function of the subunits of NOX tion in extracellular matrix (Fillinger and Elad, 2016). A variety of in B. cinerea has been extensively investigated (Siegmund et al., proteins encoded by the predicted genes were detected through com- 2013). Both the catalytic subunits BcNoxA and BcNoxB are respon- parative proteomics (Shah et al., 2009; Espino et al., 2010; Li et al., sible for pathogenicity and the formation of sclerotia, which allow 2012). However, only few of them have been confirmed to have the fungi to survive under adverse environmental conditions and are fundamental for sexual reproduction (Siegmund et al., 2015). Interestingly, BcNoxA and BcNoxB were shown to play different roles in the pathogenicity of B. cinerea (Marschall et al., 2016). BcNoxA is essential for colonizing the host tissue, whereas BcNoxB contributes to the primary infection (Segmuller et al., 2008). The regulatory subunit BcNoxR has a phenotype consistent with that of ΔbcnoxA/B double mutant. Elimination of BcNoxR showed reduced growth rate, sporulation, and impaired virulence on French bean/ tomato leaves and various fruits (Li et al., 2016). Based on the com- parative proteomic approach to unravel the potential downstream targets of BcNoxR, we identified a total of 49 unique proteins whose abundance changed in the deletion mutant of bcnoxR (∆bcnoxR) and found that BcNoxR could affect the expression of proteins with various functions, such as stress response, carbohydrate metabolism, translation, and intracellular signalling. Further analysis showed that 6-phosphogluconate dehydrogenase (BcPGD), whose abun- dance decreased in the deletion mutant of bcnoxR, was responsible for growth, sporulation, and virulence of B. cinerea (Li et al., 2016). Moreover, we observed that small GTPase BcRho3 was contributed to the regulation of mycelial growth, conidiation production, and virulence of B. cinerea, and deletion mutant of bcrho3 (∆bcrho3) showed reduced virulence to apple, tomato fruits, and tomato leaves, and proved that the reduction in virulence of ∆bcrho3 mutant might Figure 1 Model for reactive oxygen species (ROS) generation and be due to the impaired penetration ability (An et al., 2015). transportation in B. cinerea. Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/111/5057759 by Ed 'DeepDyve' Gillespie user on 28 August 2018 Pathogenic mechanisms and control strategies, 2018, Vol. 2, No. 3 113 function in the pathogenicity of B. cinerea. Two endopolygalacturo- identified proteins were proteolysis, whereas the major proteins nase (BcPG1 and BcPG2) are involved in the virulence of B. cinerea. detected at pH 6 were CWDEs (Li et al., 2012). The proteases are The Bcpg1 gene is not required for primary infection but necessary usually utilized by the fungi to degrade the structural plant cell or for further colonization on apple fruits, tomato fruits, and leaves (ten antifungal proteins secreted by the plant host (ten Have et al., 2004), Have et al., 1998), whereas Bcpg2 affects both primary infection and and CWDEs are essential for fungi to decompose plant cell wall to lesion expansion on tomato and broad bean (Kars et al., 2005a). The achieve full virulence (Kubicek et al., 2014). Moreover, we found endo-β-1,4-xylanases (BcXYN11A), which degrade plant cell wall that the production of those extracellular proteins was regulated at content xylan, were proven to have a pronounced effect on viru- the transcriptional level, suggesting that B. cinerea has the ability to lence (Brito et al., 2006). Lots of the CWDEs are demonstrated to be fine-tune its secretome according to the predominant pH conditions not essential for the virulence of B. cinerea. Pectin methyl esterase to achieve successful infection, and that it might possess complicate induces the demethylesterification of cell wall components polyga- regulatory mechanism to perceive and response to ambient pH at the lacturonans (Kars et al., 2005b). Cutinase has the potential to hydro- transcriptional level (Li et al., 2012) (Figure 2). lyse cutin, thus facilitating pathogen penetration through the cuticle The most well characterized regulatory mechanism is pal signal- (van Kan et al., 1997). However, deletion mutants of genes of pec- ling pathway (Penalva and Arst, 2002). In Aspergillus nidulans, sev- tin methylesterase (BcPME1 and BcPME2) or cutinase (BcCUTA) eral genes are involved in the pal signalling pathway, namely, PacC, exhibit no effects on the virulence of B. cinerea (van Kan et al., PalA, PalB, PalC, PalF, PalH, and PalI (Penalva et al., 2008). Under 1997). Considering the high redundancy of CWDEs, these enzymes alkaline conditions, the pH signal is sensed and transmitted from might have an overlapped function with others and contributed to the plasma membrane to the endosomal membrane by PalH, PalI, the overall pathogenicity of this fungus (Kars et al., 2005b). and PalF. When the endosomal membrane complex including PalA, The important roles of extracellular proteins necessitated a pre- PalB, and PalC receives the signal, the complex will proteolyse PacC cise regulation mechanism. Extracellular proteins usually initiate to a protease-accessible conformation. PacC will be further pro- with the process of endoplasmic reticulum (Sakaguchi, 1997), trans- cessed to its active form in a pH-independent manner. Under acidic ported to the golgi compartment for further modifications (Novick conditions, most of PacC exist in a protease-inaccessible conform- and Zerial, 1997), and then transported to the membrane by secre- ation and only trace amounts of PacC are in protease-accessible tory vesicles (Conesa et al., 2001; Stenmark and Olkkonen, 2001). conformation. PacC is a zinc finger transcription factor which will Rab family proteins, which belong to the Ras superfamily of small activate the alkaline-expressed genes and repress acid-expressed GTPase, have been extensively reported to play important roles in genes (Penalva et al., 2008). PacC has also been reported in many the secretory pathway (Novick and Zerial, 1997; Punt et al., 2001; other plant pathogens, such as Sclerotinia sclerotiorum (Rollins and Minz-Dub et al., 2013). The first identified Rab protein is SEC4 in Dickman, 2001), Alternaria alternata (Eshel et al., 2002), Fusarium yeast (Clement et al., 1998). SEC4 has been suggested to participate oxysporum (Caracuel et al., 2003), P. digitatum (Zhang et al., 2013), in the growth and protein secretion of Candida albicans (Mao et al., and Penicillium expansum (Barad et al., 2014). In B. cinerea, the 1999). The homologue of SEC4-like Rab in Aspergillus niger and gene expression of bcpacc was significantly higher at pH 6 than that Colletotrichum lindemuthianum has also been identified, namely, at pH 4, indicating its role in ambient pH response of B. cinerea (Li srgA and CLPT1 (Dumas et al., 2001). Disruption of srgA in A. niger et al., 2012). BcACP1 is a G1-family endopeptidase which only func- resulted in reduced protein secretion and abnormal apical branching tions in acid environment. Ambient pH regulates bcacp1 at both the (Punt et al., 2001). In contrast, deletion of CLPT1 in C. lindemuthi- transcriptional and post-translational levels; however, the pH regu- anum led to a lethal phenotype (Dumas et al., 2001). A mutant with lation of BcACP1 was independent of the canonical PacC binding a dominant-negative allele of CLPT1 was further used to investigate site (Rolland et al., 2009), suggesting other binding site of BcPacC or the function of CLPT1, and ascertained that CLPT1 was essential even other pH signalling pathway might exist in B. cinerea. for secretory vesicles transportation, infectious structures forma- tion, and pathogenicity (Siriputthaiwan et al., 2005). In B. cinerea, BcSAS1 was determined to be a Rab/GTPase family gene. Deletion of bcsas1 (∆bcsas1) resulted in reduced virulence in apple, tomato fruits, and tomato leaves. The ∆bcsas1 mutant exhibits an accu- mulation of trafficking vesicles at the hyphal tips. A comparative approach was applied to investigate the secretome of ∆bcsas1, and the secretion of polysaccharide hydrolases and proteases were sig- nificantly depressed (Zhang et al., 2014b). Environmental Conditions Affect Pathogenicity of B. cinerea Effect of ambient pH on pathogenicity pH is a major environmental factor that affects the interaction between B. cinerea and its hosts. Fruits usually present a pH ranging from 3.32 to 4.39, whereas leaves, stems, and roots exhibit a higher pH ranging from 5.81 to 6.3 (Manteau et al., 2003). To explore the secretome of B. cinerea on different host tissues, we chose pH 4 and 6 to mimic the pH values of fruits and other tissues, cultured B. cinerea at different pH conditions and found that distinct dif- Figure 2 Botrytis cinerea utilize different extracellular enzymes to infect hosts ferences exist in the secretome of B. cinerea. At pH 4, most of the according to the ambient pH conditions. Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/111/5057759 by Ed 'DeepDyve' Gillespie user on 28 August 2018 114 L. Hua et al. 2018, Vol. 2, No. 3 Besides adjusting an arsenal of pathogenicity factors to fit for the (Cohrs et al., 2016). BcLTF3 is another C H transcription factor 2 2 wide range of environment conditions, most fungi hold the potential with dual functions and represses conidiophore development but is to actively altering the local pH environment to fulfil its infection essential for the maturation of conidia. Deletion mutant of bcltf3 (Prusky and Yakoby, 2003; Tian et al., 2016). Fungi usually achieve produced abundant conidiophores but failed to produce mature environmental pH changes through secreting acids or alkali. The conidia (Brandhoff et al., 2017). BcLTF4-6 are Zn2Cys6 transcrip- organic acids secreted by fungi include oxalic acid, gluconic acid, cit- tion factors and exhibit no obvious roles in vegetative growth or ric acids, butyric acid, malate and succinate, whereas the alkali usu- development (Schumacher et al., 2014). The expression of BcLTF2 ally refers to ammonia (Vylkova, 2017). Botrytis cinerea has been is tightly regulated by BcLTF1, BcLTF3, BcREG1, and other pro- reported to acidify the plant tissue through secreting large amounts teins. (Brandhoff et al., 2017). BcREG1 is a transcriptional factor of oxalic acid (Manteau et al., 2003). Acidic pH environment can in previously known to be involved in the conidiogenesis and second- turn regulate the activity or expression of putative pathogenicity fac- ary metabolism in B. cinerea (Michielse et al., 2011). In recent study, tors, such as endopolygacturonase, laccase, and protease (ten Have BcREG1 was re-identified as a light-responsive transcriptional regu- et al., 1998; Wubben et al., 2000; Kars et al., 2005a; Li et al., 2012). lator which influences conidia formation by repress BcLTF2-induced An oxalate-deficient mutant of B. cinerea grew normally in vitro, conidiation in the light, while active a conidiation program inde- but failed to produce disease symptoms (Kunz et al., 2006). These pendent of BcLTF2 in the dark (Brandhoff et al., 2017), suggesting results demonstrated that B. cinerea can modulate environmental that light is a determinant factor of generating conidia or sclerotia. pH conditions via utilizing OA, thus contributing to its colonization Some of the light-responsive transcriptional factors or regu- of the host tissues. lators also function in the regulation of pathogenicity. We found that Δbcmads1 showed reduced disease symptoms on apple fruit when compared with the wild type. Based on proteomic analysis, Effects of light on pathogenicity we identified the potential downstream targets of BcMADS1, and Light is a vital environmental factor acting as energy source, signal, proved that 63 proteins changed abundance in Δbcmads1. Among and stress to various living organisms. Light responsive organisms them, two proteins (BcSEC14 and BcSEC31) were related to secre- sense light to schedule their development and adjust their adap- tion and involved in the pathogenicity of B. cinerea (Zhang et al., tion (Rodriguez-Romero et al., 2010). Botrytis cinerea is a light 2016). BcLTF1 was also demonstrated to play an important role in responsive strain that actively sense light conditions to fine-tune virulence, ROS homoeostasis, and secondary metabolism. Deletion its development and pathogenicity (Zhang et al., 2016). Light is of bcltf1 resulted in reduced virulence on bean leaves, increased an essential developmental signal for B. cinerea as it triggers exclu- ROS accumulation, and overexpression of secondary metabolism- sively formation of conidia, whereas constant darkness initiates the related genes (Schumacher et al., 2014). The light-responsive tran- solely formation sclerotia (Fillinger and Elad, 2016). Conidia and scriptional regulator BcREG1 is required for pathogenicity, and the sclerotia are two types of survival structures of B. cinerea. Conidia deletion mutant of bcreg1 is hampered in causing necrotic lesions are asexual spores produced under favourable environmental condi- though capable to penetrate plant tissue (Colmenares et al., 2002). tions and contribute to rapid growth and reproduction (Brandhoff Δbcreg1 mutant displayed reduced ability to produce phytotox- et al., 2017), whereas sclerotia are sexual spores that allow for the ins such as botryane, sesquiterpenes, and polyketides, which might fungi to survive adverse environmental conditions (Willetts, 1971). facilitate pathogenesis (Michielse et al., 2011). It is worth noting The balance between asexual and sexual development is tightly that the pathogenesis-related light-responsive transcriptional fac- regulated to ensure better survival and drive adaptive responses. tors or regulators also function in protein secretion or second Extensive studies about light regulation on the development of metabolism. In filamentous fungi, velvet proteins are among the B. cinerea have been conducted, especially those light responsive most important components coordinating light signal and sec- transcription factors. BcMADS1 is MADS-box family transcription ondary metabolism. Velvet proteins have been identified as a het- factors that play crucial roles in regulation of various cellular func- erotrimeric velvet complex VelB/VeA/LaeA in A. nidulans. VeA tions (Shore and Sharrocks, 1995; Messenguy and Dubois, 2003). physically interacts with VelB and bridges VelB to LaeA, a nuclear We found that deletion mutant of bcmads1 in B. cinerea resulted master regulator of secondary metabolism (Bayram et al., 2008). In in reduced growth rate compared with the wild type B05.10. An B. cinerea, BcVEL1/BcVEL2/BcLAE1 are, respectively, homologue always conidia phenotype which lost the ability to produce sclerotia to VelB/VeA/LaeA. BcVEL1 interacts with BcVEL2 and BcLAE1 to was observed, and the conidia formed by B. cinerea in dark was form the velvet complex (Yang et al., 2013). Deletion mutants of even higher than that produced in light (Zhang et al., 2016). The BcVEL1, BcVEL2, or BcLAE1 present similar phenotypes such as complementation strain of bcmads1 restored the sclerotia formation reduced virulence and altered secondary metabolism (Schumacher ability of Δbcmads1, indicating the function of BcMADS1 in light et al., 2015). perception and in the environment fitness of this pathogen (Zhang et al., 2016). Other six light-responsive transcription factors that are significantly induced when exposed to white light were termed Control Strategies of B. cinerea BcLTF1-6 (Brandhoff et al., 2017). BcLTF1 is a GATA transcription Due to the gigantic economic losses brought by B. cinerea, consider- factor participating in the regulation of light-dependent vegetative able strategies have been carried out to control Botrytis-incited dis- growth and differentiation. Deletion mutants of bcltf1 (Δbcltf1) lost eases, including chemical control, resistance inducer, and biological the ability to grow under light conditions on minimal medium, and control (Figure 3). the radial growth rates have a negative correction with the exposure time to light. However, Δbcltf1 forms more conidia upon exposed Chemical control to yellow light and more sclerotia under red light than wild type (Schumacher et al., 2014). BcLTF2 belongs to the C H transcription Application of synthetic fungicides to control post-harvest diseases 2 2 factor family, and the overexpression of bcltf2 is capable of switch- caused by B. cinerea is the main method in production. There are ing the conidiation program on and suppressing sclerotia generation five categories of fungicides, respectively, acting on the respiration, Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/111/5057759 by Ed 'DeepDyve' Gillespie user on 28 August 2018 Pathogenic mechanisms and control strategies, 2018, Vol. 2, No. 3 115 Figure 3 Control strategies of B. cinerea. microtubule assembly, osmoregulation, sterol biosynthesis, and Resistance inducer those whose effects can be reversed by methionine (Leroux, 2007). Some plant signalling molecules, such as salicylic acid (SA), jasmonic However, two main problems exist in the application of fungicides. acid (JA), can induce resistant of plants against fungal pathogens On one hand, Botrytis tend to change constantly during generations (Park et al., 2007; Robert-Seilaniantz et al., 2011). As substitute for as it has multinucleate conidia. Resistance strains to different catego- fungicides, they have been investigated and applied to control post- ries of fungicides are frequently discovered. For example, Botrytis harvest diseases in fresh fruits with some success (Terry and Joyce, was noted to develop resistant isolates when benzimidazole fungi- 2004; Yao and Tian, 2005; Romanazzi et al., 2016). Our previous cides were first used (Bollen and Scholten, 1971). The resistant strains results indicated that SA enhanced the resistance of sweet cherry to dicarboximides were also reported soon after (Katan, 1982). fruits against P. expansum, resulting in lower disease incidences and On the other hand, application of synthetic fungicides is expen- smaller lesion diameters, and revealed that antioxidant proteins, sive since the control of B. cinerea usually necessitates higher dose heat shock proteins, and dehydrogenases were involved in resistance rates than other fungal pathogens. The cost at control of Botrytis response of the fruits (Chan et al., 2008). Tomato fruit treated by and related species accounted for about 8 per cent of the fungicide exogenous MeJA showed higher resistance to B. cinerea infection, market worldwide (Fillinger and Elad, 2016). In addition, chemical because MeJA treatment stimulated decreased catalase (CAT) and ascorbate peroxidase (APX) gene expression and enhanced ascorbate fungicides are harmful to the environment and human beings, espe- (ASC) and glutathione (GSH) content, being beneficial for scaveng- cially their toxicological residues. Therefore, a great many of regu- ing excess ROS and alleviating oxidative damage of proteins (Zhu latory restrictions are put on the applications of botryticides (Droby and Tian, 2012). MeJA treatment induced resistance of Chinese bay- et al., 2009). Boron is an important plant micronutrient (Loomis berries against fungal pathogen by priming defense responses, and and Durst, 1992) and has been shown to be effective in control of up-regulated the hydrogen peroxide burst and enhanced translation B. cinerea (Qin et al., 2010). Boron has the potential to destroy cell levels of defence-related proteins and the contents of antimicrobial membrane and result in the leakage of cytoplasmic materials from compounds (Wang et al., 2014). Cinnamic acid is also proved to be the pathogen (Qin et al., 2010). The detailed antifungal mechanism effective in controlling gray mold rot caused by B. cinerea in table of boron against P. expansum has been investigated by comparative grape, its modes of the action include to inhibit the mycelial growth proteomics. The results indicated that there were 14 proteins related via damaging the plasma membrane integrity, and stimulate the to stress response and basic metabolism changed abundance after resistance of fruit host by inducing the activities of proteins such as treated with borate, and among them, two proteins, catalase and peroxidase and polyphenol oxidase (Zhang et al., 2015). glutathione S-transferase, were both down-regulated after borate treatment (Qin et al., 2007). One secretory protein, namely, polyga- Biological control lacturonase, which contributes to virulence in various pathogens (ten Have et al., 1998; Isshiki et al., 2001; Oeser et al., 2002; Kars et al., Utilizing living biological microbe agents to control post-harvest dis- 2005a), was also identified to be affected in the presence of borate ease is a potential technology instead of chemical fungicides (Sharma (Qin et al., 2007). et al., 2009). Our previous studies indicated that a variety of Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/111/5057759 by Ed 'DeepDyve' Gillespie user on 28 August 2018 116 L. Hua et al. 2018, Vol. 2, No. 3 Barad, S., Horowitz, S. B., Kobiler, I., Sherman, A., Prusky, D. (2014). antagonistic yeasts can effectively inhibit post-harvest decay caused Accumulation of the mycotoxin patulin in the presence of gluconic acid by B. cinerea in different fruits (Piano et al., 1997; Fan and Tian, contributes to pathogenicity of Penicillium expansum. Molecular Plant- 2001; Tian et al., 2002; Qin et al., 2004). Antagonistic yeasts are Microbe Interactions, 27: 66–77. more pursued since they are safer than bacteria as no toxic second- Bayram, O., et al. (2008). Velb/vea/laea complex coordinates light signal with ary metabolites were detected in their activities against pathogens fungal development and secondary metabolism. Science (New York, N.Y.), (Tian, 2006). Their modes of action against fungal pathogens include 320: 1504–1506. through competing the limited space and nutrients (Janisiewicz et al., Bedard, K., Lardy, B., Krause, K. H. (2007). NOX family NADPH oxidases: 2000; Chan and Tian, 2005), inducing host resistance (Navazio not just in mammals. Biochimie, 89: 1107–1112. et al., 2007; Tian et al., 2007; Hermosa et al., 2012), or producing Bienert, G. P., et al. (2007). Specific aquaporins facilitate the diffusion of hydro- cell-wall lytic enzymes which facilitate the infection of pathogens gen peroxide across membranes. The Journal of Biological Chemistry, 282: 1183–1192. (Yang et al., 2009). However, the effect of antagonistic yeasts is not Bollen, G. J., Scholten, G. (1971). Acquired resistance to benomyl and some that remarkable as fungicides and usually call for the combination of other systemic fungicides in a strain of Botrytis cinerea in cyclamen. fungicides or exogenous substances to gain a satisfying result (Droby European Journal of Plant Pathology, 77: 83–90. et al., 2009). Much work has shown that antagonistic yeasts com- Brandhoff, B., Simon, A., Dornieden, A., Schumacher, J. (2017). Regulation bined with calcium chloride (An et al., 2012), salicylic acid (Chan of conidiation in Botrytis cinerea involves the light-responsive tran- and Tian, 2006; Qin et al., 2003; Zhang et al., 2010), sodium bicar- scriptional regulators bcltf3 and bcreg1. Current Genetics, 63: bonate (Yao et al., 2004), silicon (Qin and Tian, 2005), boron (Cao 931–949. et al., 2012) and glycine betaine (Liu et al., 2011) can significantly Brito, N., Espino, J. J., González, C. (2006). The endo-beta-1,4-xylanase improve their biocontrol efficacy in control of post-harvest diseases xyn11a is required for virulence in Botrytis cinerea. Molecular Plant- in various fruits. Combination of hot water treatment with Candida Microbe Interactions, 19: 25–32. Cao, B. H., Li, H., Tian, S. P., Qin, G. Z. (2012). Boron improves the biocontrol guilliermondii or Pichia membranaefaciens showed a better control activity of Cryptococcus laurentii against Penicillium expansum in jujube efficacy against B. cinerea in tomato fruit (Zong et al., 2010). fruit. Postharvest Biology and Technology, 68: 16–21. Caracuel, Z., Roncero, M. I., Espeso, E. A., González-Verdejo, C. I., García- Conclusion Maceira, F. I., Di Pietro, A. (2003). The pH signalling transcription fac- tor pacc controls virulence in the plant pathogen Fusarium oxysporum. Botrytis cinerea is an aggressive plant pathogen, which causes gray Molecular Microbiology, 48: 765–779. mould rot in fresh horticultural crops, resulting in heavy economical Chan, Z. L., Tian, S. P. (2005). Interaction of antagonistic yeasts against post- losses in the world. Due to the genetic variety of B. cinerea, resist- harvest pathogens of apple fruit and possible mode of action. Postharvest ant strains are frequently found. It is important to reveal molecu- Biology and Technology, 36: 215–223. lar basis of pathogenicity and regulatory mechanisms of B. cinerea. Chan, Z. L., Tian, S. P. (2006). Induction of H O -metabolizing enzymes and 2 2 Current understanding indicates that ROS and extracellular proteins total protein synthesis in sweet cherry fruit by Pichia membranefaciens and salicylic acid treatment. Postharvest Biology and Technology, 39: are related to the regulation of growth, development, and virulence. 314–320. The genome sequence of B. cinerea has been released and genetic Chan, Z. L., et al. (2008). Functions of defense-related proteins and dehydro- methods such as construction of deletion mutants have been success- genases in resistance response induced by salicylic acid in sweet cherry fully used to investigate its pathogenic mechanisms. Since a few of fruits at different maturity stages. Proteomics, 8: 4791–4807. target genes involved in pathogenicity of B. cinerea have been found, Choquer, M., et al. (2007). Botrytis cinerea virulence factors: new insights into it is possible to develop and improve control technologies. However, a necrotrophic and polyphageous pathogen. FEMS Microbiology Letters, more research effectors are still needed to understanding of compre- 277: 1–10. hensive information about molecular pathogenic mechanisms and Clement, M., Fournier, H., de Repentigny, L., Belhumeur, P. (1998). Isolation regulatory network to develop more precise and effective strategies and characterization of the Candida albicans SEC4 gene. Yeast (Chichester, for prevention and control of B. cinerea. England), 14: 675–680. Cohrs, K. C., Simon, A., Viaud, M., Schumacher, J. (2016). Light governs asexual differentiation in the grey mould fungus Botrytis cinerea via the Acknowledgements putative transcription factor bcltf2. Environmental Microbiology, 18: 4068–4086. We thank National Key R&D Program of China (2016YFD0400902) and Colmenares, A. J., Aleu, J., Durán-Patrón, R., Collado, I. G., Hernández- National Natural Science Foundation of China (31530057, 31722043 and Galán, R. (2002). The putative role of botrydial and related metabolites in 31671910) to support our research work. the infection mechanism of Botrytis cinerea. Journal of Chemical Ecology, 28: 997–1005. References Conesa, A., Punt, P. J., van Luijk, N., van den Hondel, C. A. (2001). The Amselem, J., et al. (2011). Genomic analysis of the necrotrophic fungal patho- secretion pathway in filamentous fungi: a biotechnological view. Fungal gens sclerotinia sclerotiorum and Botrytis cinerea. PLOS Genetics, 7: Genetics and Biology, 33: 155–171. e1002230. Dean, R., et al. (2012). The top 10 fungal pathogens in molecular plant path- An, B., Li, B. Q., Li, H., Zhang, Z. Q., Qin, G. Z., Tian, S. P. (2016). Aquaporin8 ology. Molecular Plant Pathology, 13: 414–430. regulates cellular development and reactive oxygen species production, a Droby, S., Wisniewski, M., Macarisin, D., Wilson, C. (2009). Twenty years of critical component of virulence in Botrytis cinerea. New Phytologist, 209: postharvest biocontrol research: is it time for a new paradigm? Postharvest 1668–1680. Biology and Technology, 52: 137–145. An, B., Li, B. Q., Qin, G. Z., Tian, S. P. (2012). Exogenous calcium improves Dumas, B., et al. (2001). Molecular characterization of CLPT1, a SEC4-like viability of biocontrol yeasts under heat stress by reducing ROS accumu- rab/gtpase of the phytopathogenic fungus colletotrichum lindemuthianum lation and oxidative damage of cellular protein. Current Microbiology, which is regulated by the carbon source. Gene, 272: 219–225. 65: 122–127. Eshel, D., Miyara, I., Ailing, T., Dinoor, A., Prusky, D. (2002). pH regu- An, B., Li, B. Q., Qin, G. Z., Tian, S. P. (2015). Function of small gtpase rho3 lates endoglucanase expression and virulence of alternaria alter- in regulating growth, conidiation and virulence of Botrytis cinerea. Fungal nata in persimmon fruit. Molecular Plant-Microbe Interactions, 15: Genetics and Biology, 75: 46–55. 774–779. Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/111/5057759 by Ed 'DeepDyve' Gillespie user on 28 August 2018 Pathogenic mechanisms and control strategies, 2018, Vol. 2, No. 3 117 Espino, J. J., Gutiérrez-Sánchez, G., Brito, N., Shah, P., Orlando, R., González, phytopathogenic fungus Botrytis cinerea. FEMS Microbiology Ecology, C. (2010). The Botrytis cinerea early secretome. Proteomics, 10: 43: 359–366. 3020–3034. Mao, Y., Kalb, V. F., Wong, B. (1999). Overexpression of a dominant-negative Fan, Q., Tian, S. P. (2001). Postharvest biological control of grey mold and allele of SEC4 inhibits growth and protein secretion in Candida albicans. blue mold on apple by Cryptococcus albidus (Saito) Skinner. Postharvest Journal of Bacteriology, 181: 7235–7242. Biology and Technology, 21: 341–350. Marschall, R., Siegmund, U., Burbank, J., Tudzynski, P. (2016). Update on nox Fillinger, S., Elad, Y. (2016). Botrytis-the Fungus, the Pathogen and its function, site of action and regulation in Botrytis cinerea. Fungal Biology Management in Agricultural Systems. Pub. Springer, New York. and Biotechnology, 3: 8. ten Have, A., Dekkers, E., Kay, J., Phylip, L. H., van Kan, J. A. (2004). An Mellersh, D. G., Foulds, I. V., Higgins, V. J., Heath, M. C. (2002). H O plays 2 2 aspartic proteinase gene family in the filamentous fungus Botrytis cinerea different roles in determining penetration failure in three diverse plant- contains members with novel features. Microbiology (Reading, England), fungal interactions. The Plant Journal: for Cell and Molecular Biology, 150: 2475–2489. 29: 257–268. ten Have, A., Mulder, W., Visser, J., van Kan, J. A. (1998). The endopolyga- Messenguy, F., Dubois, E. (2003). Role of MADS box proteins and their cofac- lacturonase gene bcpg1 is required for full virulence of Botrytis cinerea. tors in combinatorial control of gene expression and cell development. Molecular Plant-Microbe Interactions, 11: 1009–1016. Gene, 316: 1–21. Heller, J., Tudzynski, P. (2011). Reactive oxygen species in phytopatho- Michielse, C. B., Becker, M., Heller, J., Moraga, J., Collado, I. G., Tudzynski, genic fungi: signaling, development, and disease. Annual Review of P. (2011). The Botrytis cinerea reg1 protein, a putative transcriptional Phytopathology, 49: 369–390. regulator, is required for pathogenicity, conidiogenesis, and the produc- Hermosa, R., Viterbo, A., Chet, I., Monte, E. (2012). Plant-beneficial effects of tion of secondary metabolites. Molecular Plant-Microbe Interactions, 24: trichoderma and of its genes. Microbiology, 158: 17–25. 1074–1085. Isshiki, A., Akimitsu, K., Yamamoto, M., Yamamoto, H. (2001). Miller, E. W., Dickinson, B. C., Chang, C. J. (2010). Aquaporin-3 mediates Endopolygalacturonase is essential for citrus black rot caused by alter- hydrogen peroxide uptake to regulate downstream intracellular signaling. naria citri but not brown spot caused by Alternaria alternata. Molecular Proceedings of the National Academy of Sciences of the United States of Plant-Microbe Interactions, 14: 749–757. America, 107: 15681–15686. Janisiewicz, W. J., Tworkoski, T. J., Sharer, C. (2000). Characterizing the Minz-Dub, A., Kokkelink, L., Tudzynski, B., Tudzynski, P., Sharon, A. mechanism of biological control of postharvest diseases on fruits with a (2013). Involvement of Botrytis cinerea small gtpases bcras1 and bcrac simple method to study competition for nutrients. Phytopathology, 90: in differentiation, virulence, and the cell cycle. Eukaryotic Cell, 12: 1196–1200. 1609–1618. van Kan, J. A., van’t Klooster, J. W., Wagemakers, C. A., Dees, D. C., van der Navazio, L., et al. (2007). Calcium-mediated perception and defense responses Vlugt-Bergmans, C. J. (1997). Cutinase A of Botrytis cinerea is expressed, activated in plant cells by metabolite mixtures secreted by the biocontrol but not essential, during penetration of gerbera and tomato. Molecular fungus Trichoderma atroviride. BMC Plant Biology, 7: 41. Plant-Microbe Interactions, 10: 30–38. Novick, P., Zerial, M. (1997). The diversity of rab proteins in vesicle transport. Kars, I., Krooshof, G. H., Wagemakers, L., Joosten, R., Benen, J. A., van Kan, Current Opinion in Cell Biology, 9: 496–504. J. A. (2005a). Necrotizing activity of five Botrytis cinerea endopolygalac- Oeser, B., Heidrich, P. M., Müller, U., Tudzynski, P., Tenberge, K. B. (2002). turonases produced in pichia pastoris. The Plant Journal: for Cell and Polygalacturonase is a pathogenicity factor in the claviceps purpurea/rye Molecular Biology, 43: 213–225. interaction. Fungal Genetics and Biology, 36: 176–186. Kars, I., McCalman, M., Wagemakers, L., van Kan, J. A. (2005b). Functional Orozco-Cárdenas, M. L., Narváez-Vásquez, J., Ryan, C. A. (2001). Hydrogen analysis of Botrytis cinerea pectin methylesterase genes by PCR-based tar- peroxide acts as a second messenger for the induction of defense genes in geted mutagenesis: Bcpme1 and Bcpme2 are dispensable for virulence of tomato plants in response to wounding, systemin, and methyl jasmonate. strain B05.10. Molecular Plant Pathology, 6: 641–652. The Plant Cell, 13: 179–191. Katan, T. (1982). Resistance to 3,5-dichlorophenyl-N-cyclic imide (‘dicarbo- Park, S. W., Kaimoyo, E., Kumar, D., Mosher, S., Klessig, D. F. (2007). Methyl ximide’) fungicides in the grey mould pathogen Botrytis cinerea on pro- salicylate is a critical mobile signal for plant systemic acquired resistance. tected crops. Plant Pathology, 31: 133–141. Science (New York, N.Y.), 318: 113–116. Kubicek, C. P., Starr, T. L., Glass, N. L. (2014). Plant cell wall-degrading Penalva, M. A., Arst, H. N. Jr. (2002). Regulation of gene expression by ambi- enzymes and their secretion in plant-pathogenic fungi. Annual Review of ent pH in filamentous fungi and yeasts. Microbiology and Molecular Phytopathology, 52: 427–451. Biology Reviews, 66: 426–446, table of contents. Kunz, C., et al. (2006). Characterization of a new, nonpathogenic mutant Penalva, M. A., Tilburn, J., Bignell, E., Arst, H. N. Jr. (2008). Ambient pH of Botrytis cinerea with impaired plant colonization capacity. New gene regulation in fungi: making connections. Trends in Microbiology, 16: Phytologist, 170: 537–550. 291–300. Leroux, P. (2007). Chemical Control of Botrytis and its Resistance to Chemical Piano, S., Neyrotti, V., Migheli, Q., Gullino, M. L. (1997). Biocontrol cap- Fungicides. Pub. Springer, The Netherlands, pp. 195–222. ability of Metschnikowia pulcherrima against Botrytis postharvest rot of Loomis, W. D., Durst, R. W. (1992). Chemistry and biology of boron. apple. Postharvest Biology and Technology, 11: 131–140. Biofactors, 3: 229–239. Pletjushkina, O. Y., et al. (2006). Hydrogen peroxide produced inside mito- Li, B. Q., Wang, W. H., Zong, Y. Y., Qin, G. Z., Tian, S. P. (2012). Exploring chondria takes part in cell-to-cell transmission of apoptotic signal. pathogenic mechanisms of Botrytis cinerea secretome under differ- Biochemistry, 71: 60–67. ent ambient pH based on comparative proteomic analysis. Journal of Prusky, D., Yakoby, N. (2003). Pathogenic fungi: leading or led by ambient ph? Proteome Research, 11: 4249–4260. Molecular Plant Pathology, 4: 509–516. Li, H., Zhang, Z. Q., He, C., Qin, G. Z., Tian, S. P. (2016). Comparative Punt, P. J., et al. (2001). Identification and characterization of a family of proteomics reveals the potential targets of bcnoxr, a putative regulatory secretion-related small gtpase-encoding genes from the filamentous fungus subunit of NADPH oxidase of Botrytis cinerea. Molecular Plant-Microbe aspergillus niger: a putative SEC4 homologue is not essential for growth. Interactions, 29: 990–1003. Molecular Microbiology, 41: 513–525. Liu, J., Wisniewski, M., Droby, S., Vero, S., Tian, S. P., Hershkovitz, V. Qin, G. Z., Liu, J., Cao, B. H., Li, B. Q., Tian, S. P. (2011). Hydrogen peroxide (2011). Glycine betaine improves oxidative stress tolerance and biocon- acts on sensitive mitochondrial proteins to induce death of a fungal patho- trol efficacy of the antagonistic yeast cystofilobasidium infirmominiatum. gen revealed by proteomic analysis. PLOS One, 6: e21945. International Journal of Food Microbiology, 146: 76–83. Qin, G. Z., Tian, S. P. (2005). Enhancement of biocontrol activity of Manteau, S., Abouna, S., Lambert, B., Legendre, L. (2003). Differential Cryptococcus laurentii by silicon and the possible mechanisms involved. regulation by ambient pH of putative virulence factor secretion by the Phytopathology, 95: 69–75. Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/111/5057759 by Ed 'DeepDyve' Gillespie user on 28 August 2018 118 L. Hua et al. 2018, Vol. 2, No. 3 Qin, G. Z., Tian, S. P., Chan, Z. L., Li, B. Q. (2007). Crucial role of anti- Stenmark, H., Olkkonen, V. M. (2001). The rab gtpase family. Genome oxidant proteins and hydrolytic enzymes in pathogenicity of Penicillium Biology, 2: REVIEWS3007. expansum: analysis based on proteomics approach. Molecular & Cellular Terry, L. A., Joyce, D. C. (2004). Elicitors of induced disease resistance in Proteomics, 6: 425–438. postharvest horticultural crops: a brief review. Postharvest Biology and Qin, G. Z., Tian, S. P., Xu, Y. (2004). Biocontrol of postharvest diseases on Technology, 32: 1–13. sweet cherries by four antagonistic yeasts in different storage conditions. Tian, S. P. (2006). Microbial control of postharvest diseases of fruits and Postharvest Biology and Technology, 31: 51–58. vegetables: current concepts and future outlook. In: Ray R. C., Ward O. Qin, G. Z., Tian, S. P., Xu, Y., Wan, Y. K. (2003). Enhancement of biocon- P. (eds.). Microbial Biotechnology in Horticulture, Vol. 1. Pub. Science, trol efficacy of antagonistic yeasts by salicylic acid in sweet cherry fruit. Enfield, pp. 163–202. Physiological and Molecular Plant Pathology, 62: 147–154. Tian, S. P., Fan, Q., Xu, Y., Liu, H. B. (2002). Biocontrol efficacy of antagon- Qin, G. Z., Zong, Y. Y., Chen, Q. L., Hua, D. L., Tian, S. P. (2010). Inhibitory ist yeasts to gray mold and blue mold on apples and pears in controlled effect of boron against Botrytis cinerea on table grapes and its possible atmospheres. Plant Disease, 86: 848–853. mechanisms of action. International Journal of Food Microbiology, 138: Tian, S. P., Qin, G. Z., Li, B. Q. (2013). Reactive oxygen species involved 145–150. in regulating fruit senescence and fungal pathogenicity. Plant Molecular Rice, M. E. (2011). H O : a dynamic neuromodulator. The Neuroscientist: Biology, 82: 593–602. 2 2 A Review Journal Bringing Neurobiology, Neurology and Psychiatry, 17: Tian, S. P., Torres, R., Ballester, A., Li, B. Q., Vilanova, L., González-Candelas, 389–406. L. (2016). Molecular aspects in pathogen-fruit interactions: virulence and Robert-Seilaniantz, A., Grant, M., Jones, J. D. (2011). Hormone crosstalk in resistance. Postharvest Biology and Technology, 122: 11–21. plant disease and defense: more than just jasmonate-salicylate antagonism. Tian, S. P., Yao, H. J., Deng, X., Xu, X. B., Qin, G. Z., Chan, Z. L. (2007). Annual Review of Phytopathology, 49: 317–343. Characterization and expression of beta-1,3-glucanase genes in jujube Rodriguez-Romero, J., Hedtke, M., Kastner, C., Müller, S., Fischer, R. (2010). fruit induced by the microbial biocontrol agent Cryptococcus laurentii. Fungi, hidden in soil or up in the air: light makes a difference. Annual Phytopathology, 97: 260–268. Review of Microbiology, 64: 585–610. Vylkova, S. (2017). Environmental pH modulation by pathogenic fungi as a Rolland, S., Bruel, C., Rascle, C., Girard, V., Billon-Grand, G., Poussereau, N. strategy to conquer the host. PLOS Pathogens, 13: e1006149. (2009). pH controls both transcription and post-translational processing Waghray, M., et al. (2005). Hydrogen peroxide is a diffusible paracrine sig- of the protease Bcacp1 in the phytopathogenic fungus Botrytis cinerea. nal for the induction of epithelial cell death by activated myofibroblasts. Microbiology (Reading, England), 155: 2097–2105. FASEB Journal, 19: 854–856. Rollins, J. A., Dickman, M. B. (2001). pH signaling in sclerotinia sclerotio- Wang, K. T., et al. (2014). Methyl jasmonate induces resistance against rum: identification of a pacc/RIM1 homolog. Applied and Environmental Penicillium citrinum in Chinese bayberry by priming of defense responses. Microbiology, 67: 75–81. Postharvest Biology and Technology, 98: 90–97. Romanazzi, G., Sanzani, S. M., Bi, Y., Tian, S. P., Gutierrez-Martinez, P., Alkan, Weiberg, A., et al. (2013). Fungal small rnas suppress plant immunity by hijack- N. (2016). Induced resistance to control postharvest decay of fruit and ing host RNA interference pathways. Science (New York, N.Y.), 342: vegetables. Postharvest Biology and Technology, 122: 82–94. 118–123. Sakaguchi, M. (1997). Eukaryotic protein secretion. Current Opinion in Willetts, H. J. (1971). The survival of fungal sclerotia under adverse environ- Biotechnology, 8: 595–601. mental conditions. Biological Reviews, 46: 387–407. Schumacher, J., et al. (2015). The VELVET complex in the gray mold fun- Williamson, B., Tudzynski, B., Tudzynski, P., van Kan, J. A. (2007). Botrytis gus Botrytis cinerea: impact of bclae1 on differentiation, secondary cinerea: the cause of grey mould disease. Molecular Plant Pathology, 8: metabolism, and virulence. Molecular Plant-Microbe Interactions, 28: 561–580. 659–674. Wubben, J. P., ten Have, A., van Kan, J. A., Visser, J. (2000). Regulation of endopol- Schumacher, J., Simon, A., Cohrs, K. C., Viaud, M., Tudzynski, P. (2014). ygalacturonase gene expression in Botrytis cinerea by galacturonic acid, ambi- The transcription factor bcltf1 regulates virulence and light responses in ent pH and carbon catabolite repression. Current Genetics, 37: 152–157. the necrotrophic plant pathogen Botrytis cinerea. PLOS Genetics, 10: Yang, Q., Chen, Y., Ma, Z. (2013). Involvement of bcvea and bcvelb in regu- e1004040. lating conidiation, pigmentation and virulence in Botrytis cinerea. Fungal Seaver, L. C., Imlay, J. A. (2001). Hydrogen peroxide fluxes and compartmen- Genetics and Biology, 50: 63–71. talization inside growing Escherichia coli. Journal of Bacteriology, 183: Yang, H. H., Yang, S. L., Peng, K. C., Lo, C. T., Liu, S. Y. (2009). Induced prote- 7182–7189. ome of trichoderma harzianum by Botrytis cinerea. Mycological Research, Segmuller, N., Kokkelink, L., Giesbert, S., Odinius, D., van Kan, J., Tudzynski, P. 113: 924–932. (2008). NADPH oxidases are involved in differentiation and pathogenicity Yao, H. J., Tian, S. P. (2005). Effects of a biocontrol agent and methyl jas- in Botrytis cinerea. Molecular Plant-Microbe Interactions, 21: 808–819. monate on postharvest diseases of peach fruit and the possible mecha- Shah, P., Atwood, J. A., Orlando, R., El Mubarek, H., Podila, G. K., Davis, M. nisms involved. Journal of Applied Microbiology, 98: 941–950. R. (2009). Comparative proteomic analysis of Botrytis cinerea secretome. Yao, H. J., Tian, S. P., Wang, Y. S. (2004). Sodium bicarbonate enhances bio- Journal of Proteome Research, 8: 1123–1130. control efficacy of yeasts on fungal spoilage of pears. International Journal Sharma, R. R., Singh, D., Singh, R. (2009). Biological control of posthar- of Food Microbiology, 93: 297–304. vest diseases of fruits and vegetables by microbial antagonists: a review. Zhang, Z. Q., Li, H., Qin, G. Z., He, C., Li, B. Q., Tian, S. P. (2016). The Biological Control, 50: 205–221. MADS-box transcription factor Bcmads1 is required for growth, scler- Shore, P., Sharrocks, A. D. (1995). The MADS-box family of transcription fac- otia production and pathogenicity of Botrytis cinerea. Scientific Reports, tors. European Journal of Biochemistry, 229: 1–13. 6: 33901. Siegmund, U., Heller, J., van Kan, J. A., van Kann, J. A., Tudzynski, P. (2013). Zhang, H., et al. (2010). Enhancement of biocontrol efficacy of Rhodotorula The NADPH oxidase complexes in Botrytis cinerea: evidence for a close glutinis by salicyclic acid against gray mold spoilage of strawberries. association with the ER and the tetraspanin pls1. PLOS One, 8: e55879. International Journal of Food Microbiology, 141: 122–125. Siegmund, U., Marschall, R., Tudzynski, P. (2015). Bcnoxd, a putative ER Zhang, Z. Q., Qin, G. Z., Li, B. Q., Tian, S. P. (2014a). Infection assays of protein, is a new component of the NADPH oxidase complex in Botrytis tomato and apple fruit by the fungal pathogen Botrytis cinerea. Bio- cinerea. Molecular Microbiology, 95: 988–1005. Protocol, 23: e1311. Siriputthaiwan, P., Jauneau, A., Herbert, C., Garcin, D., Dumas, B. (2005). Zhang, Z. Q., Qin, G. Z., Li, B. Q., Tian, S. P. (2014b). Knocking out Bcsas1 Functional analysis of CLPT1, a rab/gtpase required for protein secretion in Botrytis cinerea impacts growth, development, and secretion of extra- and pathogenesis in the plant fungal pathogen colletotrichum lindemuthi- cellular proteins, which decreases virulence. Molecular Plant-Microbe anum. Journal of Cell Science, 118: 323–329. Interactions, 27: 590–600. Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/111/5057759 by Ed 'DeepDyve' Gillespie user on 28 August 2018 Pathogenic mechanisms and control strategies, 2018, Vol. 2, No. 3 119 Zhang, Z. Q., Qin, G. Z., Li, B. Q., Tian, S. P. (2015). Effect of cinnamic acid Zhu, Z., Tian, S. P. (2012). Resistant responses of tomato fruit treated by for controlling gray mold on table grape and its possible mechanisms of exogenous methyl jasmonate to Botrytis cinerea infection. Scientia action. Current Microbiology, 71: 396–402. Horticulturea, 142: 38–43. Zhang, T. Y., Sun, X. P., Xu, Q., Candelas, L. G., Li, H. Y. (2013). The pH sign- Zong, Y. Y., Liu, J., Li, B. Q., Qin, G. Z., Tian, S. P. (2010). Effects of yeast aling transcription factor PacC is required for full virulence in Penicillium antagonists in combination with hot water treatment on postharvest dis- digitatum. Applied Microbiology and Biotechnology, 97: 9087–9098. eases of tomato fruit. Biological Control, 54: 316–321. Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/111/5057759 by Ed 'DeepDyve' Gillespie user on 28 August 2018
Food Quality and Safety – Oxford University Press
Published: Sep 1, 2018
Access the full text.
Sign up today, get DeepDyve free for 14 days.