Agriculture (Poľnohospodárstvo), 67, 2021 (2): 47 − 60 Review DOI: 10.2478/agri-2021-0005 1,2* 1,2 2 MICHAELA HAVRLENTOVÁ , JÁN KRAIC , VERONIKA GREGUSOVÁ , BERNADETT KOVÁCSOVÁ National Agricultural and Food Centre, Lužianky, Slovak Republic University of Ss. Cyril and Methodius, Trnava, Slovak Republic Havrlentová, M., Kraic, J., Gregusová, V. and Kovácsová, B. (2021). Drought stress in cereals – A review. Agriculture (Poľnohospodárstvo), 67(2), 47 – 60. Drought is one of the most important factors that influences plant morphology, biochemistry, and physiology, and finally leads to the decline in crops productivity and seed quality. Climate change, severe changes in water availability together with thermal stresses environment coincide with increasing human population, and to reveal sustainable solutions it is necessary to understand: i) how cereals react to drought, ii) how the tolerance mechanisms are exhibited by the genotype, and iii) which approaches enable to increase the tolerance of crop species against limited water availability. Especially in cereals as in high-quality food sources, it is important to reveal the adaptation mechanisms to rainfall dynamics on arable land and to the prolonged period of drought. This review summarizes current knowledge on the impact of drought on cereals, the mechanisms these crops utilize to cope water scarcity and survive, and the most efficient approaches to improve their drought tolerance. Key words: drought, wheat, dehydrins, abscisic acid, reactive oxygen species, photosynthesis al. 2017), quality in agriculture and threaten food 1. INTRODUCTION (Fedoroff et al. 2010; Parkash & Singh 2020). Plants live in a constantly changing environment The impact of abiotic stress continues to have that often affects their growth and development. dominant effects on crop production (Lobell et al. They adapt to life under stress conditions by adjust- 2011), whereby only 3.5% of the total land area on ing their physiology, morphology, or metabolism to Earth is unaffected by environmental factors (FAO minimize stress-induced damages. Changes to the 2013). Studies have shown that over the next 30 plant’s biochemical and physiological processes ul- years, the Earth’s average surface temperature will timately causing damage to death are considered to increase by about 0.2°C over a decade. It is estimat- plant stress (Atkinson & Urwin 2012). Drought, sa- ed that the increase in average global temperature linity, and temperature are the major environmental will increase by 2.5 to 4.5°C on average by the end factors, which affect the geographical distribution of the 21st century due to increasing concentrations and productivity of plants (Wang et al. 2003; Sara- of greenhouse gases (such as CO , N O, and CH ) 2 2 4 dadevi et al. 2017; Siddiqui et al. 2017; Ghatak et in the atmosphere (Wang et al. 2018). The Food and Michaela Havrlentová (*Corresponding author), Ján Kraic, National Agricultural and Food Centre, Research Institute of Plant Production, Bratislavská cesta 122, 921 68 Piešťany, Slovak Republic. E-mail: email@example.com, jan. firstname.lastname@example.org Michaela Havrlentová, Ján Kraic, Veronika Gregusová, Bernadett Kovácsová, University of Ss. Cyril and Methodius, Faculty of Natural Sciences, Department of Biotechnologies, Nám. J. Herdu 2, 917 01 Trnava, Slovak Republic. E-mail: michaela. email@example.com, firstname.lastname@example.org, email@example.com, firstname.lastname@example.org © 2021 Authors. This is an open access article licensed under the Creative Commons Attribution-NonComercial-NoDerivs License (http://creativecommons.org/licenses/by-nc-nd/4.0/). 47 Agriculture (Poľnohospodárstvo), 67, 2021 (2): 47 − 60 Agriculture Organization (FAO) reported in 2018 assimilation, cellu- water relations, decreased CO that 83% of the damage and loss in agriculture as lar oxidative stress, membrane damage of affected a share of total damage and loss across all sectors tissues, and in some cases, inhibition of enzymes in years 2006 – 2016 was caused by drought (FAO activity. Under drought conditions, plants can alter 2018). water relations to maintain cellular functions. For Most the plants have very little ability to cope example, plants exhibit osmotic adjustment by syn- with the environmental conditions in a short term thesizing and accumulating compatible solutes such and are extremely vulnerable to acute water short- as free amino acids, sugars, and proline (edit some ages. references) (Izanloo et al. 2008; Tatar & Gevrek Wheat (Triticum aestivum L.) as the world’s 2008). Osmotic adjustment allows the plant to main- most important cereal crop is grown in a large range tain turgor pressure and cell volume at low water of latitudes worldwide under both irrigated and rain- potential which is important for maintaining met- fed conditions and thus in conditions subjected to abolic functions. In addition, osmotic adjustment drought. Wheat is considered as an excellent sys- facilitates the recovery of metabolic activities after tem to study drought tolerance in spite of its genetic relief from stress (Izanloo et al. 2008). complexity (Cheng et al. 2016). Although investigations have been made to study the recovery of photosynthesis from drought stress (Osakabe et al. 2014) in different crop species in- 2. PHYSIOLOGICAL CHANGES IN cluding wheat, studies addressing membrane sta- CEREALS DURING DROUGHT bility, oxidative stress, antioxidative process, and osmolyte dynamics during drought recovery are Water scarcity occurs during drought, where wa- limited. Studies quantifying the impact of plant met- ter is simply not present in the soil. Physiological abolic changes during drought indicate, that stress drought is not necessarily caused only by a lack of conditions during vegetative growth periods can water in the soil, but it can also occur when there significantly influence grain yield of wheat (Araus is an excess of water (the soil water potential is et al. 2002; Souza et al. 2004; Siddiqui et al. 2017). lower than in the plant) or high soil salinity (ions After drought stress is removed, the availability of also affect the water potential). Thus, physiolog- even a small amount of rainfall can have a signifi- ical drought is a condition where the plant cannot cant effect on plant physiological functions, ranging receive water (Lisar et al. 2012; Osakabe et al. from whole-plant physiological and morphologi- 2014). The responses of plants to water stress are cal responses to biochemical responses (Abobatta diverse and may involve the contribution of various 2019). Therefore, it is of particular importance to defence mechanisms or modification of physiology, investigate the underlying mechanisms contributing morphology, anatomy, biochemistry, as well as short to drought tolerance (Izanloo et al. 2008). and long-term developmental and growth-related Water deficit in plants decreases or suppresses the adaptation processes (Abobatta 2019). process of photosynthesis (Earl & Davis 2003; An- Physiological responses to drought and heat jum et al. 2011; Kapoor et al. 2020). The decrease in stresses providing an escape to the water or heat the photosynthetic process under drought is mainly conductance via stress comprise morphological and physiological attributable to the decline in CO stomata and mesophyll limitations, however, the de- adjustments (Lamaoui et al. 2018). Enlarged root crease in photosynthetic activity due to drought may system (Gregorová et al. 2015; Abobatta 2019), re- also be due to reduced ability of stomatal movement duced stomatal number and conductance, decreased (Abid et al. 2018). The loss of CO uptake affects leaf area, increased leaf thickness, and leaf rolling Rubisco activity and decrease the function of nitrate or folding (Earl & Davis 2003) to lessen evapotrans- reductase and sucrose phosphate synthase and the piration (Anjum et al. 2011; Lamaoui et al. 2018; ability for ribulose bisphosphate (RuBP) production Kapoor et al. 2020) are strictly associated with an (Singh & Thakur 2018). adaptive response. Reduced plant growth and pro- The chlorophyll content is another photosyn- ductivity under drought are caused by altered plant 48 Agriculture (Poľnohospodárstvo), 67, 2021 (2): 47 − 60 thetic attribute strongly influenced by water deficit soil layers by boosting their root architecture (Mitra (Gregorová et al. 2015; Alghbari & Iksan 2018). For 2001; Lisar et al. 2012; Abobatta 2019). The main example, leaf chlorophyll synthesis and chlorophyll basis of variation appears to be constitutive, there- a/b proportion is altered by drought stress. A decline fore, a root system architecture that allows reserve in photosynthetic activity, amount of chlorophylls, of more water quantity is the most important tool loss of photosystem II photochemical efficiency, al- for drought tolerance (Abobatta 2019). Moreover, teration in stomatal movement, and disturbance in water availability is primarily recognized by roots, the water status of plants resulted in declined plant which in turn regulates its growth (Kudoyarova et productivity. Among others, a major cause for the al. 2011). decline in the amount of chlorophyll due to drought The plant leaf is an important part of the plant 2− stress is the drought-promoted O and H O pro- because of the process of photosynthesis, which in 2 2 duction, which results in lipid peroxidation and turn is the main driver of plant growth. Decrease in significant chlorophyll degradation. Drought stress leaf area is a drought avoidance strategy because also causes a reduction in the abundance of several declining leaf area results in a decreased water loss Calvin cycle proteins, including Rubisco (Anjum et by the process of transpiration (Earl & Davis 2003; al. 2011). Anjum et al. 2011; Kapoor et al. 2020) and this re- In terms of metabolites, a reduced rate of photo- duction in leaf area is attributable to the inhibition synthesis disrupts carbohydrate production, lowers of leaf expansion by the declined rate of cell divi- the level of sucrose in leaves, and prevents the trans- sion, which results in loss of cell turgidity (Xu et port of sucrose into organs. Ultimately, reproductive al. 2010). development is limited. In addition, drought induces Abiotic stress will typically cause upper and vacuolar inverse of sucrose mediated by hydrolysis lower spikelets and distil florets to either abort or and modulation of osmotic potential. Drought inhib- produce small grains (Nuttall et al. 2017). A re- its the cell division of the developing embryo/endo- duction in grain filling occurs due to a reduction in sperm resulting in the poor intensity of cell division the assimilate partitioning and activities of sucrose and ultimately leading to germ abortion (Andersen and starch synthesis enzymes (Farooq et al. 2009), et al. 2002). however, the period and duration of the stress fac- tor is important. Following heading, drought had 2.1 Effect of drought on plant growth little effect on the rate of kernel filling in wheat, Drought stress is well recognized as a limiting but its duration (time from fertilisation to maturity) factor that alters multiple aspects of plant growth was shortened, and dry weight reduced at maturity and development (Alghbari & Iksan 2018; Kapoor (Wardlaw & Willenbrink 2000). In barley, drought et al. 2020). Germination of seeds, health, coleop- stress reduces grain yield by reducing the number of tile length, and leaf area are foremost for the plant tillers, spikes, grains per plant, and individual grain progression. Seed germination is the primary aspect weight. Post-anthesis drought stress was detrimental of growth that is sensitive to drought (Kapoor et to grain yield regardless of the stress severity (Sama- al. 2020). Visible symptoms of the plant exposed rah 2005; Alghbari & Iksan 2018). In durum wheat, to water scarcity in the initial vegetative stage is thousand-grain weight, grain protein yield, and test besides seed germination reduction also leaf wilt- weight reduced significantly under both salinity and ing. Plant growth is also in term of reducing shoot drought stress conditions, whereby salinity stress length and fresh weight of the hypocotyls negative- was greater than drought stress (Houshmand et al. ly affected by lack of water (Abobatta 2019). The 2014). interruption in establishment of buds and flowers Soil water deficit condition reduces crop yield by is also observed due to a lack of nutrients from the reducing the plant growth according to the follow- dried soil (Abobatta 2019; Kapoor et al. 2020). The ing three main mechanisms: i) reduction in canopy root system is the main plant organ for adaptation absorption of photosynthetically active radiation, ii) to drought stress conditions. In conditions of wa- decreased radiation use efficiency, and iii) decreased ter deficit, plants seek to extract water from deeper harvest index (Earl & Davis 2003). 49 Agriculture (Poľnohospodárstvo), 67, 2021 (2): 47−60 2.2 Effect of drought on seed quality gallanes-López et al. 2017). Salt and drought stress Drought stress leads to the yield losses of ma- in another work with durum wheat grown for two jor crops worldwide every year (Wang et al. 2003; years on the field experiment caused the significant Saradadevi et al. 2017; Siddiqui et al. 2017). Reduc- increase in grain protein content, wet and dry gluten ing the availability of water during drought results contents, and SDS-sedimentation volume, whereby in a reduction in total nutrient intake and nutrients the impact of salinity stress was greater than drought concentration in plant tissues. A significant impact stress (Houshmand et al. 2014). Flour protein con- of the water deficit is manifested in the transport tent and SDS sedimentation volume increased, but from the perception point, namely from the root not significantly, under drought stress conditions in system to the above-ground parts (Garg 2003). In durum wheat in the work of Li et al. (2013). In con- general, drought stress induces an increase in nitro- trast, the gluten strength-related parameters such as gen content (Li et al. 2013; Alghabari et al. 2018; lactic acid retention capacity and mixograph peak Magallanes-López et al. 2017; Kapoor et al. 2020), time increased significantly under drought. Drought a definite decrease in phosphorus levels, and does also significantly enhanced flour yellowness (Li et not have significant end effects on potassium con- al. 2013). tent (Garg 2003). During booting and anthesis stag- es in winter wheat cultivation in a pot experiment 3. MAIN MECHANISMS OF A PLANT TO under drought stress the concentration of nitrogen ADAPT TO DROUGHT CONDITIONS and sulphur were observed higher for dwarf culti- vars, whereas no significant differences were ob- The common drought-responsive mechanism served between tall and semi-dwarf wheat cultivars comprises several characteristics: 1) Drought es- (Alghabari et al. 2015). cape via completing plant life cycle before severe Starch synthesis is highly sensitive to high tem- water stress conditions (e.g., early flowering) (Lisar perature and drought stress. Its accumulation in et al. 2012; Abobatta 2019). 2) Drought avoidance wheat grains can be reduced by over 30% after heat via enhancing water taking capacity (e.g., develop- treatment, at temperatures between 30°C and 40°C. ing root systems or conserving water by reducing Thus, the ability to synthesize, store, and remobilize transpiration such as closure/reduction of stomata starch at high temperature is crucial for the determi- and leaf area). 3) Drought tolerance via improving nation of grain sink strength (Ni et al. 2018). The osmotic adjustment and increasing cell wall elas- effects of abiotic stress on the dietary fibre content ticity to maintain tissue turgidity. 4) Drought resis- of wheat and barley grains appear to be variable as tance via altering metabolic pathways under severe one report suggests that β-glucan content of bar- water stress condition. 5) Drought abandonment by ley decreases under high temperature and drought reducing/removing a plant part (e.g., shedding ma- stress (Savin et al. 1997), whereas another reports an increase in β-glucan content under drought stress ture leaves) (Prasad et al. 2017). 6) Drought-prone (Jansen et al. 2013). biochemical-physiological traits for plant evolution In durum wheat (Triticum turgidum L. var. du- under long-term drought condition via genetic mu- rum) drought stress affect grain yield, which led to tation and genetic modification (Xu et al. 2010). All an increase in protein content by linking with better these mechanisms may be involved consecutively or gluten strength and better bread-making quality in simultaneously in plant responses to drought stress the drought environment, although other traits relat- (Xu et al. 2010; Han et al. 2015). Generally, C3 ed to gluten quality and content as sodium dodecyl plants are better adapt to drought, because the re- is more posi- sulfate- (SDS)-sedimentation or mixograph mixing sponse of C3 species to increased CO tive than that of C4 species thanks to increased pho- time were somewhat lower in that environment, tosynthetic rate (Araus et al. 2002; Hamim 2005). which indicates probably qualitative changes at the Increased CO increases the water use efficiency of protein level (Li et al. 2013; Magallanes-López et C3 species because it causes a reduction in transpi- al. 2017). The analysis of the glutenins composition ration rate and an increase in CO assimilation rate confirmed different effects of some alleles (Ma- 50 Agriculture (Poľnohospodárstvo), 67, 2021 (2): 47 − 60 of the plants (Hamim 2005). Studies have also sug- tions and also in their stomatal sensitivity to ABA. gested that C3 species may obtain more benefits of Root density distribution in the upper drying layers CO enrichment under drought stress (Ward et al. of the soil profile is identified as a candidate trait 1999; Hamim 2005). that can affect ABA accumulation and subsequent One of the most important molecules and best stomatal closure (Daszkowska-Golec & Szarejko investigated in stress signalling is the plant hormone 2013; Saradadevi et al. 2017). A simple collection abscisic acid (ABA) (Davies et al. 2005; Daszkow- of leaf samples to quantify ABA compared to ex- ska-Golec & Szarejko 2013; Takahashi et al. 2020). tracting xylem tissue will facilitate rapid screening Endogenous ABA is rapidly produced in the plant of a large number of germplasm for drought toler- during drought and triggers a cascade of physiolog- ance (Saradadevi et al. 2017). ical reactions, including stomatal closure (Davies et An increased concentration of ABA in leaves as- sociated with reduced stomatal conductance under al. 2005) which is regulated by a signal transduction water deficits has been confirmed in several studies network. Stomatal activity, which is influenced by conducted in various species including wheat (Sara- environmental stress factors, can affect the absorp- dadevi et al. 2017). A higher concentration of ABA tion of CO and thus affect photosynthesis and plant was observed in wheat roots in association with in- growth (Osakabe et al. 2014). creased root hydraulic conductance following exci- Among proteins, heat-shock proteins (HSPs) (Di sion of four out of five seminal roots. This increased Donato & Geisler 2019) and dehydrins (Kosová et concentration of ABA in root and subsequent en- al. 2013) are involved in plant responses to a drought hancement of root hydraulic conductivity to meet stress reaction. Chitinases (EC 188.8.131.52) and gluca- increased transpiration demand is due to the redis- nases (EC 184.108.40.206) are other molecules activated tribution of ABA from leaf to root (Kudoyarova et in wheat by drought. Individual isoforms and their al. 2011). Thus, leaf ABA is involved in regulating activity were rather stimulated under drought, espe- root hydraulic conductivity, in addition to its role in cially in shoots (Gregorová et al. 2015). regulating stomata (Saradadevi et al. 2017). 3.1 Effect of ABA in cereals during drought condi- ABA has a central role in root-to-shoot drought tions stress signalling (Davies et al. 2005; Takahashi et Regulation of ABA under drought in plants is al. 2020) and the regulation of functioning, growth, well discussed in many studies (Davies et al. 2005; and development of plants in drying soil (Davies et Daszkowska-Golec & Szarejko 2013; Ghatak et al. al. 2005). Changes in xylem and apoplastic pH can 2017; Takahashi et al. 2020). However, the detailed affect the way in which ABA regulates stomatal be- molecular mechanisms of stress sensors and the reg- haviour and growth (Davies et al. 2005). ulators that initiate ABA biosynthesis in response The lack of consensus among researchers in re- to drought stress conditions are still unclear (Taka- lation to a positive, negative, or neutral influence of hashi et al. 2020). ABA on grain yield suggests that the timing at which Plant roots reflect to the drying soil and produce the water stress occurs is important. Pre-anthesis wa- signals, while ABA on transmission to shoots trig- ter stress, particularly during spike development and gers stomatal closure to regulate crop water use pollen meiosis, reduces grain number while post-an- through transpiration. However, transpiration is thesis water stress reduces grain size (Dolferus et al. linked to crop growth and productivity, and limit- 2011). This is because high ABA levels during the ing transpiration may reduce potential yield. While early reproductive stage affect grain composition an early and high degree of stomatal closure affects and reduce grain number. On the other hand, during photosynthesis (Osakabe et al. 2014) and hence post-anthesis stages, high ABA levels promote grain biomass production, a late and low degree of sto- filling by redistributing reserved carbohydrates to matal closure exhausts available soil water rapidly the grain (Liu et al. 2005). In one of the recent stud- which results in yield losses through a reduction in ies, when the soil water was exhausted rapidly after post-anthesis water use. Wheat genotypes differ in anthesis, the wheat cultivar Drysdale maintained their ability to produce ABA under drought condi- a higher grain yield with a higher harvest index and 51 Agriculture (Poľnohospodárstvo), 67, 2021 (2): 47 −60 grain weight compared to the advanced drought-tol- turnover of its substrates, the so-called client pro- erant line IGW-3262. This was mainly because the teins (Di Donato & Geisler 2019). cultivar Drysdale was more efficient at transloca - 119 DnaJ (HSP40) proteins (TaDnaJs; encoded tion of assimilates to grain (Saradadevi et al. 2015). by 313 genes) and 41 HSP70 proteins (TaHsp70s; Based on this study it appears that ABA negatively encoded by 95 genes) have been identified and clas- affects grain composition, but has a positive effect sified in wheat into six and four groups, respective - on grain filling by facilitating assimilate distribution ly, via a phylogenetic analysis. An examination of to grain (Saradadevi et al. 2017). protein sequence alignment revealed diversity in the TaDnaJ structural organization, but a highly con- 3.2 The importance of HSPs in plant protection served J-domain characterized by an HPD motif fol- during drought lowed by DRD or DED motifs was observed (Guo Heat shock proteins (HSPs) are a major compo- et al. 2021). In the work of Kumar et al. (2020) us- nent of multiple stress responses in plants (Guo et ing Position-Specific Scoring Matrix (PSSMs) and al. 2021; Kumar et al. 2020). HSPs are controlled by sequence homology 753 TaHSPs including 169 by the action of diverse heat shock factors which are TaSHSP (small HSP), 273 TaHSP40, 95 TaHSP60, activated under stress conditions (Maaroufi & Tan- 114 TaHSP70, 18 TaHSP90, and 84 TaHSP100 were guay 2013; Jacob et al. 2017). By definition, protein denaturation is a constant identified in the wheat genome. Compared with oth- direct or indirect consequence of any stress, as er grass species, the number of HSPs in wheat is rel- stresses are defined as factors limiting normal cel- atively high probably due to the higher ploidy level lular functions carried out by proteins (Atkinson & and a large number of tandem duplication was iden- Urwin 2012). Potentially, any stressor that induc- tified in TaHSPs, especially TaSHSPs. The TaHSPs es protein misfolding would require HSPs. There- genes show random distribution on chromosomes, by, chaperones are considered as powerful buffers however, there are more TaHSPs in B and D sub-ge- against protein misfolding during environmental nomes as compared to the A sub-genome (Kumar et stress (including drought) and consequent genetic al. 2020). variations (Carey et al. 2006; Maaroufi & Tanguay Information about the involvement of HSPs in 2013). The importance of HSPs is not limited to heat drought stress signalling is rare, however high ex- stress management, but these molecules are also pression of TaSHSP was observed during seed de- involved in other stresses, such as cold, osmoses, velopment, especially during the grain filling stage drought, salt, UV, high light, oxidative stress, and (Kumar et al. 2020). It was found that both the over- pathogen infection (Swindell et al. 2007; Maaroufi expression of HSC70 and the use of a dominant-neg- & Tanguay 2013; Di Donato & Geisler 2019; Ku- ative form of HSP90 disrupt ABA-mediated stoma- mar et al. 2020; Guo et al. 2021). ta closure, thereby negatively affect water loss in The main inducers of chaperones are heat-shock stress conditions (Di Donato & Geisler 2019). The factors (HSFs) and the diversity of the HSFs family impact of ABA treatment on HSC70, HSP90, SGT1 in plants causes their study difficult. However, se- (co-chaperone of HSP90, suppressor of G-two al- quence and expression pattern comparisons showed lele of Skp1), and RAR1 (co-chaperone of HSP90, both distinct and overlapping functions in stress re- required for Mla12 powdery mildew resistance) was sistance and development. The amount of free HSPs investigated by quantitative polymerase chain reac- is the sensor of the cell capacity to maintain a stable tion (qPCR). A decrease in SGT1a mRNA and an in- proteome and feeds back on its own production. In- crease in HSC70-4 mRNA was observed. HSC70-1 deed, in unstressed tissues, the commonly accepted and HSC70-4 must therefore share the same func- “chaperone titration model” specifies that HSFs are tion regarding the regulation of ABA signalling sequestered by HSP70/90 and maybe other chap- under physiological conditions. Only HSC70-4 is erones (Jacob et al. 2017). The HSP90 chaperone involved in mitigating ABA signals (Clement et al. machinery controls multiple cellular processes by regulating the maturation, stability, activity, and 2011). 52 Agriculture (Poľnohospodárstvo), 67, 2021 (2): 47 −60 3.3 Dehydrins activation in cereals during drought retic mobility, as it was described for Dhn4 (Kosová Dehydrins are significantly disordered proteins et al. 2014). The authors report that the gene expres- which are produced under water stress conditions. sion is an indicator of drought stress and an appro- They play an essential role in the response of plants priate adaptation mechanism and the demonstration to abiotic stress and in adapting them to the stress of drought stress increases with the exposure time conditions (Kosová et al. 2013; Thomas 2015). during the vegetative period and during the critical Their higher accumulation is usually induced in phases of plant development (Kosová et al. 2014; vegetative plant tissues under various stress factors Klimešová et al. 2017). that cause cell dehydration including salinity, lack 3.4 Importance of antioxidants in plant protection of water, cold, and frost (Kosová et al. 2013). Sev- against drought eral physiological studies oriented in plant response In wheat, several studies have reported changes to stress have shown a positive relationship between in the activity of many enzymes of the antioxidant the level of accumulation of transcripts or dehydrin defence system to control oxidative stress induced proteins and plant tolerance to stress, especially in by environmental stresses. The enzymatic compo- wheat and barley (Hordeum vulgare L.) (Kosová et nents comprise several antioxidant enzymes, such al. 2013; Vítámvás et al. 2019). as superoxide dismutase, catalase, glutathione per- The structural physicochemical and functional oxidase, guaiacol peroxidase, peroxiredoxins, and characterization of plant dehydrins and how their enzymes of the ascorbate-glutathione cycle, such properties can be used to improve resistance to as ascorbate peroxidase, monodehydroascorbate stress in plants has been described (Hanin et al. reductase, dehydroascorbate reductase, and glu- 2011). Dehydrins can non-specifically bind proteins tathione reductase (Caverzan et al. 2016; Prasad and membranes contributing to the protection of et al. 2017; Jiang et al. 2019; Kapoor et al. 2020). their functions and structure from damage caused by Non-enzymatic components include the major cel- environmental stresses. Dehydrins can also bind the lular redox buffers ascorbate and glutathione as DNA and act by not only protecting but also repair- well as tocopherols, carotenoids, and phenolic com- ing the molecule under the attack of environmental pounds. Alterations in the activity of superoxide stress factors (Liu et al. 2017). dismutase, ascorbate peroxidase, catalase, glutathi- Drought induces cell dehydration and expres- one reductase, and guaiacol peroxidase and in the sion of several dehydrins in wheat and barley. In reactive oxygen species (ROS) concentration were durum wheat, the accumulation of YSK2 dehydrin reported in wheat plants in a field and at laborato - DHN5 was studied in two cultivars exposed to ry conditions (Caverzan et al. 2016; Cheng et al. drought stress. A different pattern of phosphoryla- 2016; Jiang et al. 2019). Furthermore, many reports tion was observed in both studied cultivars, where demonstrate that the effect of abiotic stress in wheat the drought-tolerant cultivar reveals higher ranges is genotype-specific, where some genotypes show of phosphorylation than the sensitive one (Kosová different responses in the same stress condition. et al. 2014). Phosphorylation is associated with the Drought-tolerant genotypes generally maintained different subcellular localization of the protein af- a higher antioxidant capacity resulting in lower ox- fecting the final function of the protein (Kosová et idative damage (Devi et al. 2012; Caverzan et al. al. 2014). Quantitative and qualitative differences in 2016). Wheat responses also depend on the tissue low molecular weight dehydrin proteins were found type, length, and intensity of the stress as well as on in two barley cultivars with different drought toler- the developmental stage proving the complexity of ance capacity when plants were exposed to reduced the mechanisms of production and detoxification of field water capacity (Škodáček & Prášil 2011). ROS and the effect of ROS on antioxidant systems. Qualitative differences in accumulated dehydrin Many studies have reported an increase in the con- proteins may be due to either the accumulation of O after exposure to a stress and its centration of H different low molecular weight Dhn genes or allelic 2 2 production dependents on the intensity and duration variants of the same genes, which differ in copy of the stress factor (Alexieva et al. 2001; Caverzan number of hydrophilic Φ segments and electropho- 53 Agriculture (Poľnohospodárstvo), 67, 2021 (2): 47 −60 et al. 2016; Jiang et al. 2019). for determining the intracellular level of ROS, be- Furthermore, the H O level differs between sides changes in the balance of these appear to in- 2 2 various cellular compartments and is related to the duce compensatory mechanisms. type of stress (Caverzan et al. 2016; Dikilitas et al. The expression of wheat glutathione peroxidase 2020). The observed increase in enzymatic activities (GPX) genes was altered when wheat plants were and decrease in oxidative damage are closely relat- exposed to salt, H O , and ABA treatment. More- 2 2 ed. The expression of many antioxidant enzymes over, other findings suggest that GPX not only acts is positively correlated with higher tolerance lev- as scavengers of H O to control abiotic stress re- 2 2 els against abiotic stresses. The activation of some sponses but also plays important roles in salt and enzymes leads to plant protection against oxidative ABA-signalling cascades (Zhai et al. 2013). In damage. In rice plants, an important cereal model, plants, the GPX proteins are distributed in mito- increased concentration of antioxidant enzymes and chondria, chloroplasts, and the cytosol (Caverzan et increased expression levels of related genes have al. 2016). been connected with the plant response to drought ROS are well recognized for playing a dual role, (Caverzan et al. 2016). both as malignant as well as beneficial, depending on their concentration in the plant. The role of ROS as Superoxide dismutases (SODs) are a family of signalling molecules includes also processes relat- key antioxidant enzymes that play a crucial role in ed to growth, cell cycle, development, senescence, plant growth and development and are regulated by programmed cell death, stomatal conductance, and development, tissue- type, and environmental sig- hormonal signalling (Inze et al. 2012; Caverzan nals (Jiang et al. 2019). In drought stress, SODs rep- et al. 2016). H O is considered a signalling mol- resent a frontline in the defence against ROS, they 2 2 (superoxide radical) ecule in plants that mediates responses to various catalyse the dismutation of O to H O (Gill et al. 2015). Catalases (CATs) are biotic and abiotic stresses. The biological effect of 2 2 abundantly, but not exclusively, localized in peroxi- H O is related to several factors, such as the site 2 2 somes and their function is to remove the H O by of production, the developmental stage of the plant, 2 2 reducing H O to two molecules of H O. Drought-in- and its concentration (Wahid et al. 2007; Petrov & 2 2 2 duced H O accumulation is in a correlation with de- Breusegem 2012). Thus, due to the property that in 2 2 creases in soil water content and CO assimilation. low concentrations the H O acts as a stress signal, 2 2 2 Leaf H O content increases even though total CAT many studies have demonstrated that its application 2 2 activity doubling under severe drought conditions. can induce stress tolerance in plants (e.g., He et al. Drought decreases abundance and modifies the pat- 2009; Caverzan et al. 2016; Jiang et al. 2019; Diki- tern, of CAT1 and CAT2 mRNAs. The abundance of litas et al. 2020). Low H O treatments improve 2 2 CAT1 transcripts is regulated by circadian controls seed germination, seedling growth, and resistance that persist in continuous darkness, while CAT2 is to abiotic stresses (Caverzan et al. 2016). In wheat, modulated by light (Luna et al. 2005). it was observed that seed pre-treatment with H O 2 2 In wheat, a mutant line with reduced thylakoid enhances the drought tolerance of seedlings (He et ascorbate peroxidases (APXs) activity leads to re- al. 2009). The exogenous H O treatment also pro- 2 2 gress in photosynthesis (Danna et al. 2003). Rice tects wheat seedlings from damage by salt stress and mutants double silenced for cytosolic APXs exhibit seeds pre-treatment enhances salt tolerance of wheat high guaiacol peroxidase activity, which can contrib- seedlings and decreases oxidative damage (Wahid ute to the cytosolic H O scavenging in the vacuoles et al. 2007). In rice plants, H O not only acts as 2 2 2 2 or apoplasts (Bonifacio et al. 2011). APXs catalyse a toxic molecule, but also as a signalling molecule the conversion of H O into H O and use ascorbate associated with salinity, cadmium, and ABA stresses 2 2 2 as a specific electron donor. APXs proteins are dis- (Kao 2014). In wheat, H O plays an important role 2 2 tributed in chloroplasts, mitochondria, peroxisomes, as a signal molecule, but also as a harmful chemical and cytosol. The APXs genes show different modu- (Ge et al. 2013; Dikilitas et al. 2020). lation by several abiotic stresses in plants. The bal- Metabolic analyses at the level of phenolics ance between SODs, CATs, and APXs is important showed an increase in the free and bound fraction 54 Agriculture (Poľnohospodárstvo), 67, 2021 (2): 47 − 60 of phenolic acids almost exclusively in the shoots, perception. In addition, signal transduction and hor- and flavonoid isoorientin increased considerably as mone-dependent regulation pathways are also dif- a protective action against oxidative stress (Grego- ferent in various wheat genotypes. The drought-tol- rová et al. 2015). erant genotype can quickly sense drought and trig- ger the signal transduction pathways for activation of downstream elements for survival from drought 4. BIOCHEMICAL RESPONSES TO stress (Cheng et al. 2016). DROUGHT IN CEREALS During drought stress, plant cells accumulate 5. MOLECULAR TOOLS FOR soluble substances, contributing to a higher viscos- IMPROVEMENT OF DROUGHT ity in the cytoplasm. The content of these special TOLERANCE IN CEREALS substances may become toxic under certain condi- tions and may cause problems in the formation of Drought tolerance is not a qualitative trait, but enzymes and the whole process of photosynthesis a complex of quantitative plant traits controlled by (Danna et al. 2003; Han et al. 2015). In a short-term numerous genes and other plant traits with minor drought, Rubisco is relatively stable and it decom- individual effects (Senapati et al. 2018). In recent poses just after a few days. Fixed-binding inhibitors years, knowledge about molecular regulation has may reduce the activity of the Rubisco within 24 been generated to understand drought stress re- hours. The rapid decrease in “dry” photosynthesis sponses. For example, information obtained by tran- is accompanied by a reduction in the maximum rate scriptome analysis has enhanced our knowledge and of ribulose-1,5-carboxylate, the rate of regeneration facilitated the identification of candidate genes that of ribulose-1,5-bisphosphate, Rubisco, phosphoe- can be utilized for plant breeding. On the other hand, nolpyruvate carboxylase, NADP-malic enzyme, it becomes more evident that the translational and fructose-1,6-bisphosphatase, and orthophos- post-translational machinery plays a major role in phate-dikinase pyruvate (Reddy et al. 2004; Zhou et stress adaptation, especially for immediate molecu- lar processes during stress adaptation. Therefore, it al. 2007). In addition, noncyclic electron transport is is essential to measure protein levels and post-trans- reduced to meet the requirements for reduced NA- lational protein modifications to reveal information DPH production, thereby reducing ATP and ROS about stress-inducible signal perception and trans- synthesis (Reddy et al. 2004). Different cultivars within crop species may duction, translational activity, and induced protein strongly differ in their response and adaptation to levels (Ghatak et al. 2017). Research in transcrip- drought stress (Abid et al. 2018). Studies at the tran- tomics, proteomics, and metabolomics is increased scriptomic level have revealed that the drought-tol- to understand the mechanisms of drought tolerance erant and sensitive wheat genotypes can adopt dif- in plants (Swindell et al. 2007). ferent molecular strategies to overcome with drought Proteomics has become the most direct and pow- stress. One of the main differences is the differential erful tool to obtain protein expression information expression of some drought-inducible genes for cell of plants responses to drought stress, thereby com- protection (e.g., antioxidants, detoxifiers, dehydrins, plementing transcriptomic studies. Comparative transporters, and compatible solutes), regulation proteomics of drought-tolerant and sensitive wheat (e.g., kinases, transcription factors, and hormones), genotypes is a strategy to understand the complexi- and remodelling of cellular components (e.g., mem- ty of molecular mechanism in wheat in response to brane systems, cell wall, and primary metabolic net- drought stress (Cheng et al. 2016). Dehydrins have works). A large number of these genes are often ac- been reported as important factors in stress tolerance tivated in drought-sensitive wheat genotype, while and the genetic locations of some dehydrin family a tolerant genotype shows a constitutive expression members co-locate with QTL for drought tolerance of several genes activated in a sensitive genotype in barley (Thomas 2015). Of the antioxidant compo- and that contribute to limiting drought effects and nents, TaSOD genes are involved in the regulation 55 Agriculture (Poľnohospodárstvo), 67, 2021 (2): 47 − 60 of wheat tissue development and likely play import- and genes encoding them to help the plants to cope ant role in response to abiotic stress including a lon- with abiotic stresses (Ahmed et al. 2020). Many ger duration of drought. Four of these genes (Ta- genes participating in drought stress response have SOD1.1a, TaSOD1.4, TaSOD2.1, and TaSOD2.3) been already identified and transferred into cul - showed up-regulation in leaf and five genes (Ta - tured plants, including the most important cereals. SOD1.7, TaSOD1.9, TaSOD1.11a, TaSOD2.1, and Transgenic wheat, barley, maize, rice, and other TaSOD2.3) showed up-regulation in the root (Jiang cereals with increased water use efficiency and et al. 2019). drought tolerance were experimentally developed Efforts to improve crops tolerance to drought (Gao et al. 2005; Napolean et al. 2018; Zhou et and associated soil salinity are considerable, espe- al. 2018; González et al. 2019; Khan et al. 2019; cially in the context of climatic change and irriga- Oladosu et al. 2019). However, an only a very lim- tion water scarcity. Using the combination of DNA ited number of drought-tolerant cereal cultivars fingerprints of different genotypes with phenotypic created by genetic transformation are so far reg- measurements, specific chromosomal regions – so- istered for commercial use. The most important called quantitative trait loci (QTL) – were associ- databases of approved genetically modified plants ated with the expressed traits. Specific DNA mark- managed by the International Service for the Ac- ers have been linked with favourable QTLs using quisition of Agri-Biotech Applications (ISAAA’s the technology of marker-assisted selection (MAS) GM Approval Database, http://www.isaaa.org/ (Tuberosa & Salvi 2006). Thanks to the advances gmapprovaldatabase/) and the European Commu- in next-generation sequencing, the identification of nity register of GM food and feed (https://ec.eu- major QTLs regulating specific drought responses ropa.eu/food/plant/gmo/eu_register_en) include is successful and via the development of large num- at present time only drought tolerant genetically bers of genetic markers such as single nucleotide modified maize, sugarcane, and soybean. Drought polymorphisms (SNPs) and insertion-deletions tolerance of maize was obtained by the introduc- (InDels) it represents an efficient way to improve tion of the gene cspB that encodes the cold shock drought tolerance in cereal crops (Kole et al. 2015). protein B. The cspB transgene maintains normal Studies reporting major drought-responsive genes cellular functions under water stress conditions in and QTLs in wheat have recently been published the plant by preserving RNA stability and transla- (Choudhary et al. 2019; Khadka et al. 2020; Pang tion. et al. 2020) suggesting that for the past decade, Another co-solution of abiotic stress problem QTL has been the focal target of research to identify in plants is a better understanding of interactions the genetic loci regulating the adaptive response of between plants and plant growth-promoting mi- crops to drought stress (Zenda et al. 2020). croorganisms (PGPM). They can protect plants In addition to the classical and molecular plant from the negative effects of drought and salinity breeding techniques, the key tool became the trans- (Khan et al. 2020; Ma et al. 2020). Biotechnolo- fer of genes and gene regulatory regions related to gy and gene transfer technologies could increase plant water management. Transgenic approaches the effectiveness of plant-microorganism interac- using candidate genes such as transcription factors, tions. Genetically engineered PGPM enhance the microRNAs, as well as genome editing technology survival of plants under water deficiency as it has have been well summarized (Tuberosa & Salvi 2006; already been proven in plants colonized by genetic Abdallah et al. 2015; Paul & Roychoudhury 2018; engineered soil bacteria over-producing trehalose Jha 2019; Anwar & Kim 2020). Attractive targets (Vílchez et al. 2016). of plant genetic engineering for drought tolerance Biotechnology tools and genetic engineering are considered transcription factors (e.g. WRKY, approaches, along with a better understanding of MYB, NAC, AP2/ERF, GBF3). Their potential in plants, and other stress mitigation strategies, are the engineering of stress-tolerant monocot plants solutions for the very near future crop production has been already reviewed (e.g., Javed et al. 2020). with limited water resources. The subjects of interest are also signal molecules 56 Agriculture (Poľnohospodárstvo), 67, 2021 (2): 47 − 60 6. CONCLUSIONS duction, the greatest advances in the development of plants tolerant of drought and other abiotic stresses Plant responses to stress are dynamic process- have been made through genetic engineering tech- es, which are able to enhance tolerance/resistance nologies. mechanisms and establish metabolic homoeostasis under extreme environmental conditions. Regulato- Acknowledgements: This work was supported ry proteins play an important role in regulating the by the Slovak Research and Development Agency alterations under water deficit conditions and rep- (projects APVV-18-0154 and APVV-17-0113) and resent some of the most important targets for crop and by the Operational Programme Integrated In- improvement. Protein phosphorylation plays an frastructure within the project: Sustainable smart important role in signal perception and transduc- farming systems taking into account the future chal- tion under drought stress. Several kinases and phos- lenges 313011W112, cofinanced by the European phatases, and other signalling proteins are regulated Regional Development Fund. leading to stress adaptation and possible tolerance mechanisms like stomata closure. Stress acclimati- 7. REFERENCES zation is an energy-consuming process which is in- dicated by alterations in energy metabolism. 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Agriculture – de Gruyter
Published: Jul 1, 2021
Keywords: drought; wheat; dehydrins; abscisic acid; reactive oxygen species; photosynthesis