Engineering abiotic stress response in plants for biomassproductionPublished, Papers in Press, January 16, 2018, DOI 10.1074/jbc.TM117.000232

Rohit Joshi‡1, Sneh L. Singla-Pareek§2, and Ashwani Pareek‡¶2,3

From the ‡Stress Physiology and Molecular Biology Laboratory, School of Life Sciences, Jawaharlal Nehru University, New Delhi110067, India, §Plant Stress Biology, International Centre for Genetic Engineering and Biotechnology, Aruna Asaf Ali Marg,New Delhi 110067, India, and the ¶UWA Institute of Agriculture, School of Agriculture and Environment, University ofWestern Australia, Perth, Western Australia 6009, Australia

Edited by Joseph M. Jez

One of the major challenges in today’s agriculture is to achieveenhanced plant growth and biomass even under adverse envi-ronmental conditions. Recent advancements in genetics andmolecular biology have enabled the identification of a complexsignaling network contributing toward plant growth and devel-opment on the one hand and abiotic stress response on the otherhand. As an outcome of these studies, three major approacheshave been identified as having the potential to improve biomassproduction in plants under abiotic stress conditions. Theseapproaches deal with having changes in the following: (i) plant–microbe interactions; (ii) cell wall biosynthesis; and (iii) phyto-hormone levels. At the same time, employing functional genom-ics and genetics-based approaches, a very large number of geneshave been identified that play a key role in abiotic stress toler-ance. Our Minireview is an attempt to unveil the cross-talk thathas just started to emerge between the transcriptional circuit-ries for biomass production and abiotic stress response. Thisknowledge may serve as a valuable resource to eventually cus-tom design the crop plants for higher biomass production, in amore sustainable manner, in marginal lands under variable cli-matic conditions.

Despite considerable success in crop improvement pro-grams, farmers still lose almost 20 –70% of their potential cropyield because of biotic and abiotic stresses (1). Abiotic stressesare one of the key challenges for plant growth and agriculturalproductivity in arable lands, with an estimated annual loss ofbillions of dollars (2, 3). This challenge is expected to growenormously with the proposed expansion of agricultural activ-ities in less fertile and marginal areas, which is now becoming

crucial in satisfying the growing food demands (4). Becauseabout 86% of the fresh water is utilized for the production ofagricultural biomass, additional pressure is likely to develop onthe freshwater resources with the ongoing shifts from the era of“fossil energy” to the era of “energy from biomass” (5). To keeppace with this alarming situation, novel approaches are vital toenhance plant biomass production under adverse environmen-tal conditions (6).

The acclimation of plants to abiotic stress is a complex andcoordinated response involving hundreds of genes and theirinteractions with various environmental factors throughout thedevelopmental period of the plant (7–9). Accordingly, a thor-ough understanding of the molecular responses in plants isessential for targeting any improvement in plant biomass oryield. In addition, identifying suitable phenotypes that respondto multiple abiotic stresses appearing either simultaneously orsequentially under field conditions is indeed a tedious task, butit is the need of our time (10). However, to minimize the “yieldgap” caused by these abiotic stresses, it is vital to understand thegene regulatory networks operating in plants. We hope that therecent advances in molecular biology, including tissue-specificor developmental stage-specific gene expression, stringentlyregulated and induced gene expression, site-specific integra-tion of the transgene, and gene pyramiding will assist us inenhancing the photosynthetic efficiency in plants contributingeventually to produce higher biomass when grown under mar-ginal lands (11).

The development of human civilization is inextricably linkedto plant biomass, where wood and fiber are used for numerouspurposes, including energy production, textiles, paper-makingas well as bioenergy resources in the form of biofuels. As oftoday, there is a tremendous increase in the demand for plantbiomass production due to the expanding human population,inadequate food availability, and the need for bioenergy (12).However, with the ongoing debate on “food versus fuel,” weneed to reassess the options and the resources available to us.Even if we plan to use biofuels to satisfy the 20% of the growingdemand for oil products, there will be nothing left to eat. Keep-ing this fact in mind, it is imperative to design our future foodcrops that will have the potential to give high yield and biomasseven under marginal lands.

Biomass accumulation in plants occurs either by an increasein cell number or by cell expansion (13, 14). Dissecting out the

This work was supported by the International Atomic Energy Agency (Vienna,Austria), University Grants Commission-Resource Networking Center(UGC-RNW), and University with Potential for Excellence (UPE-II) (India).This is the third article in the Thematic Minireview series “Green biologicalchemistry.” The authors declare that they have no conflicts of interest withthe contents of this article.

1 Recipient of a Dr. D. S. Kothari Postdoctoral Fellowship from UGC, Govern-ment of India.

2 Supported by funding from the Indo-US Science and Technology Forum(IUSSTF) for Indo-US Advanced Bioenergy Consortium (IUABC).

3 To whom correspondence should be addressed: Stress Physiology andMolecular Biology Laboratory, School of Life Sciences, Jawaharlal NehruUniversity, New Delhi 110067, India. Tel.: 91-11-2670-4504; E-mail:ashwanip@mail.jnu.ac.in.

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regulatory network involved in cell wall biosynthesis providesan attractive strategy to improve plant architecture and bio-mass (15, 16). In recent years, considerable attention has alsobeen given to plant cell wall polymers, which form a majorcomponent of plant biomass. The composition and amount ofthese polymers in the cell wall change with plant developmentand in response to stress conditions (17). Furthermore, there isa need to delineate the genes responsible for the biosynthesis ofdifferent cell wall components, along with the assembly and theregulation of cell wall dynamics and heterogeneity (17). In addi-tion to the above strategy, manipulating endogenous plant hor-mone content provides still another possibility for improvingabiotic stress tolerance as well as biomass of plants. The thirdcrucial area to be explored for plant biomass enhancement andsustainable agriculture is “plant–microbe interaction.” Plantroots and microorganisms interact and compete for nutrients,making a complex system within the rhizosphere (18). How-ever, a complete understanding is needed regarding the effect ofthese microbes in improving abiotic stress tolerance and ininducing higher biomass production in plants (Table 1) (19).

One of the goals of our Minireview is to understand the cru-cial strategies being developed to engineer abiotic stressresponse and to enhance biomass production in plants. Here,the focus is on the above three major strategies that can beutilized to mitigate abiotic stress response, besides enhancingbiomass production. In this Minireview, we present severalexamples where plant–microbe partnerships have been utilizedto cope with the abiotic stress response leading to higher bio-mass production. Furthermore, we discuss recent advances inmolecular studies that reveal key transcriptional switches reg-ulating secondary wall biosynthesis under abiotic stress. Wealso highlight the key facets of the plant growth regulators hav-ing a direct role in the regulation of plant growth under variousabiotic stresses. The knowledge of these master switches willsimultaneously improve our understanding to develop newstrategies to genetically modify the composition and quan-

tity of lignocellulosic biomass besides increasing abioticstress tolerance.

Exploiting plant–microbe interactions

Several studies have demonstrated that plant–microbe inter-actions influence abiotic stress tolerance along with growth andbiomass. Plants form highly complex and diverse associationswith co-evolved microbial communities (20). Microbial com-munities show plant specificity in terms of their morphologyand secondary metabolism (21). Diverse mechanisms havebeen proposed for varied associations of plant growth–promoting bacteria (PGPB)4 and fungal endophytes, after theircolonization in the rhizosphere/endosphere of plants (22). Theplant–microbe interactions significantly affect carbon seques-tration, nutrient cycling, plant growth, and productivity (23, 24)besides ameliorating plant responses against abiotic stresses(22). Many studies have shown that diverse bacterial species,belonging to different genera, contribute toward toleranceagainst various abiotic stresses to the host plants resulting inenhanced biomass (25).

There is now good evidence from recent agricultural prac-tices that the use of plant growth–promoting bacteria is astrong, viable, and vital option for overcoming productivityconstraints besides mitigating environmental stresses in crops,e.g. soybean, barley, maize, and rice (26). On the one hand, themicrobes induce local or systemic inducible response mecha-nisms in plants to overcome abiotic stress, and on the otherhand, they contribute toward sustaining the biomass andgrowth through uptake, mobilization, and synthesis of nutri-ents. Hormones such as auxins, cytokinins, and gibberellinsalong with other organic compounds that stimulate cell growth

4 The abbreviations used are: PGPB, plant growth–promoting bacteria; ABA,abscisic acid; ACC, 1-aminocyclopropane-1-carboxylic acid; BR, brassinos-teroid; CK, cytokinin; GA, gibberellin; IAA, indole acetic acid; NCED, 9-cis-epoxycarotenoid dioxygenase.

Table 1Representative list of abiotic stress-responsive genes that have been genetically manipulated to improve the biomass production in plants

Target plant Gene name Observed parameter/trait Refs.

Plant microbe interactionsSolanum lycopersicum ACCD Improved plant growth in the presence of abiotic stresses 32Brassica napus ACCD Improved salt tolerance and plant growth 33

Cell wall biosynthesisArabidopsis thaliana CesA1 Higher cellulose accumulation and improved stress tolerance 40, 41A. thaliana, Oryza sativa BRI1 Enhanced drought tolerance with higher root and shoot biomass 42, 43Gossypium sp. Susy, UGPase Enhanced drought tolerance, cellulose accumulation, and total biomass 44A. thaliana XTH3 Enhanced xyloglucan biosynthesis and water stress tolerance 46Glycine max EXPB2 Improved root system architecture under water deficit 47Rosa sp. NAC2, EXPA4 Silencing of these genes resulted in reduced drought tolerance 48Zea mays CCR Inhibited wall extensibility under water stress 49A. thaliana MYB41, MPS Enhanced salt stress and cell wall biosynthesis 51A. thaliana TOR1,2 Regulation of organ and cell size, seed production, and resistance to osmotic stress 52Medicago sativa MYB46 Increased lignin deposition, secondary cell wall thickness, and enhanced abiotic stress

tolerance69

Phytohormone regulationO. sativa CKX2 Increased panicle branching with more filled grains per plant and higher harvest index

under salinity58

Arachis hypogaea IPT Enhanced biomass and yield under drought and salinity 60, 63M. sativa, A. thaliana SPL8/9 Enhanced biomass and tolerance towards salt and drought stress 67A. thaliana HDC1 Overexpression of reduced NaCl and ABA sensitivity and showed increased biomass 69Solanum lycopersicum ABRC1 Maintained growth and yield besides tolerating cold, drought, and salt stress 71Arachis hypogaea, S. lycopersicum NCED1/3 Enhanced biomass besides drought and salt stress tolerance 75, 76M. sativa, A. thaliana GSK1 Stunted growth and abiotic stress sensitivity 80

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and division under various environmental stresses have alsobeen implicated in such complex interactions (27). A schematicdiagram depicting the complex interaction of PGPB in increas-ing plant growth and biomass under stress is shown in Fig. 1.Various PGPBs possess not only the ability to induce reactiveoxygen species-scavenging enzymes but also to increase thephotosynthetic efficiency of plants under abiotic stress, thusleading to enhanced plant growth (28). Seed priming with thesePGPB strains significantly improves biomass and nutrientuptake under stress conditions (29). Recently, the multifacetedaction of microorganisms has been shown by Khan et al. (30),where enhanced expression of antioxidant enzyme machinerythrough Bacillus pumilus inoculation led to improved growthunder high-salt and boron stress in rice. Furthermore, PGPBshelp plants through phytoremediation of excessive salts, lead-ing to improved biomass production under salt stress (31). Bac-teria, such as Pseudomonas spp., Burkholderia caryophylli, andAchromobacter piechaudii, were shown to reduce endogenousethylene levels in plants by producing 1-aminocyclopropane-1-carboxylic acid (ACC)-deaminase, thus resulting in increasedroot growth and improved tolerance of salt and water stress(Table 1) (31). In addition, synthesis of indole acetic acid (IAA)or enhancing ACC deaminase activity in the rhizosphere byTrichoderma atroviride or Pseudomonas putida in tomatoresults in improved growth and stress tolerance (32). Similarly,knocking down the expression of the ACCD gene fromTrichoderma asperellum showed reduced root elongation incanola seedlings, suggesting its role in root growth promotion(33). Burkholderia phytofirmans strain PsJN improves leaf area,chlorophyll content, photosynthetic rate, and water-use effi-ciency, ultimately resulting in the enhanced shoot and root bio-mass under various abiotic stresses in a wide spectrum of hostplants, including potato, tomato, and grapevine (34).

Considerable progress has been made in unraveling themorphological, physiological, and molecular mechanisms ofgrowth-promoting bacteria-mediated abiotic stress toler-ance in plants (35). However, delineating the signaling mol-ecules released by PGPB that enhance plant growth and

defense responses still remains a challenge. Similarly, exten-sive research on enhancing the effectiveness and consistencyof microbial inoculants in multiple-stress ameliorationunder field conditions will help us in the screening of suita-ble bio-inoculants to improve crop productivity under dif-ferent environmental vagaries (36). Certainly, novel bacte-rial strains must be tested in the future to gain better insightinto the plant–microbe interaction to achieve this target.However, encompassing different “omics” approaches tostudy microbe-mediated stress mitigation strategies willfurther strengthen our knowledge on the mechanisms ofplant–microbe interactions with the naturally associated orartificially inoculated microorganisms. Primary targets foroptimizing beneficial plant–microbe interactions includequorum sensing, bacterial motility, biofilm formation, andtheir signaling pathways. Current evidence supports theplant–microbe interaction in mitigating abiotic stressresponse during varied edaphic and climatic conditions. Atpresent, a range of bacterial formulations are already avail-able commercially for their use as “bioprotection agents” or“biofertilizers” to improve biomass and yield under bioticstresses. Utilizing these microorganisms will furtherenhance tolerance against various abiotic stresses, thusestablishing novel and promising techniques for sustainableagriculture.

Regulation of cell wall biosynthesis

Around 430 million years ago, vascular plants appeared onland and co-evolved with the ability to develop a secondary cellwall. Plant cell wall functions as an “exoskeleton” by providingmechanical and structural support to the entire cell as well asacting as a physical barrier against abiotic and biotic stresses(17, 37). The principal components of a secondary cell wall arecellulose, hemicelluloses, and lignin; interestingly, they arequite unique to each cell type and vary in their amount andcomposition along with development and in response to vari-ous biotic and abiotic stresses (17, 37). Thus, we can concludethat plants have inherently evolved intricate mechanisms to

Figure 1. Plant microbe interactions for biomass enhancement. Shown is a schematic diagram representing the plant-associated bacteria that canpromote plant growth by producing various volatile organic compounds, phytohormones, siderophores, biofertilizers, and antioxidants that indirectly ordirectly benefit plant growth by induced systemic resistance, phytoremediation, systemic acquired resistance, ion chelation, nutrient acquisition, and inhibi-tion of reactive oxygen species to improve stress tolerance in host plants.

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regulate biosynthetic pathways for cell wall components andhave assembled them for the proper functioning of the cell. Forexample, plants show higher production of lignin biosynthesisenzymes during abiotic stresses (37). Similarly, severe dwarfingand altered wood anatomy were observed by silencing 4-coumarate– coenzyme A ligase, which reduces the lignin con-tent in tracheal elements (38). At present, there is fair interest inunraveling the molecular processes regulating secondary walldevelopment in plants as it is the most abundant plant biomassin the form of fiber and timber (39).

Immense progress has been made for the identification andfunctional validation of cell wall polysaccharide biosyntheticgenes (including those for cellulose, glucomannan, xyloglucan,xylan, and pectin), as well as sugar nucleotide donors of thesepathways (Table 1) (17). In plants, cellulose microfibrils, com-posed of �-1,4-glucan chains, mainly contribute toward theabove-ground biomass, and their biosynthesis and accumula-tion play a vital role in providing defense against climatic vaga-ries (40). CesA (cellulose synthase) gene superfamily regulatesthe synthesis of cellulose in plants (40). Brassinosteroid signal-ing activates the BES1 (BRI1-EMS-Suppressor-1) transcriptionfactor, which binds to the E-box (CANNTG) in the promoter ofCesA causing its up-regulation and thus resulting in enhancedcellulose accumulation in Arabidopsis (41). Similarly, CESA1kinase activity was shown to be enhanced by the degradation ofits inhibitor BRASSINOSTEROID INSENSITIVE2 (BIN2) (42).In addition, introgression of the BR receptor containing chro-mosome segment (7DL) from Agropyron elongatum resultsin enhanced drought tolerance in wheat (43). However, anincrease in UDP-Glc (a substrate for synthesis of various sugars,necessary for different wall polymers) levels by overexpressingsucrose synthase (SuSy) and UDP-glucose pyrophosphorylase(UGPase)-encoding genes leads to enhanced drought toleranceand cellulose accumulation (44). Similarly, heavy metal stress inrice and wheat causes enhanced lignin accumulation in the cellwall, which improves defense response against biotic and abi-otic stresses (45).

Transgenic Arabidopsis plants overexpressing CaXTH3,encoding a xyloglucan biosynthesis gene (xyloglucan endo-transglucosylase/hydrolases), have abnormal leaf morphologyand severely wrinkled leaf shape and enhanced toleranceagainst water stress (46). �-Expansin encoding gene EXPB2showed higher expression under water stress and seemed to beinvolved in improvement of root system architecture underwater deficits in soybeans (47). Similarly, silencing of NAC2 orits downstream gene EXPA4 has been shown to result inreduced drought tolerance during the petal development inrose (48). In contrast, overexpression of RhEXPA4 conferred animproved phenotype with shorter stems, curly leaves, compactinflorescences, and enhanced drought tolerance in Arabidopsis(48). However, higher transcript abundance of cinnamoyl-CoAreductase in maize inhibited cell wall extensibility and rootgrowth under water deficiency (49). Similarly, expansin acts asa key component in heat stress tolerance as its higher expres-sion in Agrostis leads to increased cell wall elasticity, whichmaintains cellular functions (50). Arabidopsis MYB41 and riceR2R3-type MYB transcription factor MPS (MULTIPASS) areinduced under salinity, which then enhances expression of cell

wall biosynthesis genes, during vegetative and reproductivestages, while suppressing the transcript of expansin and endo-glucanase genes (51). Similarly, overexpression of TOR, a Ser/Thr kinase of the phosphatidylinositol 3-kinase-related kinasefamily leads to enhanced cellular biomass and stress tolerance(52). However, AtTOR RNAi lines show high sensitivity towardosmotic stress (52).

Integrating the knowledge of key regulatory genes with theircell-specific promoters and transcriptional regulation of sec-ondary cell wall biosynthesis through the cascade of activators,repressors, and feedback regulators is expected to enable thedevelopment of designer plants with enhanced biomass understress conditions (16, 17). A schematic diagram depicting thetranscriptional regulatory network modulating secondary cellwall formation in plants is shown as Fig. 2. These studies alsoprovide deep insight into the complex transcriptional machin-ery to genetically modify cell wall composition for toleranceagainst abiotic stresses.

Manipulation of phytohormone levels

Of the various factors regulating plant biomass productionunder abiotic stresses, manipulation of plant hormone contentis the most efficient approach (53). Of these hormones, auxins,cytokinins (CKs), gibberellins (GAs), BRs, and abscisic acid aremarkedly involved in the regulation of plant growth and bio-mass production during stress conditions (53). Fig. 3 depictsthe cross-talk between various phytohormones leading toenhanced stress tolerance resulting in higher biomass produc-tion in plants. Dissecting the molecular mechanism of thesehormone biosyntheses and regulations provides an insight intothe complexity of various processes such as time, rate, andextent of cell division and cell expansion to manipulate theregulation of meristematic division and plant growth understress conditions (Table 1) (54). Although CKs have an impor-tant role in delaying the natural senescence in many plants (55),the concentration of the bioactive CKs decreases during expo-sure to water and salt stresses (56).

Plants exhibiting negative regulation of cytokinin activity,such as plants overexpressing CKX (cytokinin oxidase) ormutation in the cytokinin receptors, show smaller shoot api-cal meristem and decreased leaf area (57). Similarly, it isknown that knocking down CKX2 expression in rice resultsin the maintenance of photosynthetic rate, panicle branching, andreduction in yield gap under salinity stress conditions (58). Most ofthe studies on transgenic plants with pSARK promoter-regulatedisopentenyltransferase gene expression have reported delayed leafsenescence, higher photosynthetic activity, and enhanced biomassand/or yield-related parameters under drought stress in tobacco(59), rice (60), broad bean (61), and creeping bent grass (62), pea-nut (63), and under salt stress in cotton (64).

Under heavy metal and salt stress, IAA increases shoot aswell as root growth in plants (27). Transgenic poplars overex-pressing an abiotic stress-responsive YUCCA6 gene, which isinvolved in tryptophan-dependent IAA biosynthesis path-way using stress-inducible SWPA2 promoter, exhibit rapidshoot elongation and reduced main root development withenhanced root hair formation (65). Earlier studies demon-strated that down-regulation of SPL8 (squamosa promoter-

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binding-like protein-8) transcription factor significantlyincreased branching by promoting axillary bud developmentand enhanced forage biomass yield, besides enhancing saltand drought tolerance in alfalfa (66); these transgenic plantsshowed reduced GA accumulation, whereas spl8 mutantsshowed significantly higher GA transcript abundance. Fur-thermore, GA2-ox6, which is the prime GA deactivationenzyme, is significantly up-regulated by SPL8 (66). Theseresults suggest that SPL8 regulates GA signaling, andGA2-ox is a possible key node of this signaling network (67).Under saline conditions, GA application improved stomatalconductance, water use efficiency, and growth and yield intomato plants, thus supporting the above hypothesis (68).

The Arabidopsis homolog of RXT3 (REGULATOR ofTRANSCRIPTION 3), named HISTONE DEACETYLASECOMPLEX1 (HDC1) shows direct interaction with histonedeacetylases HDA6 and HDA19 (69). The hda6, hda19, andhdc1-1 mutant showed hypersensitivity toward NaCl and ABAduring seedling stage (69). However, HDC1 overexpressionreduces NaCl and ABA sensitivity and increases biomass (70).Transgenic tomato plants overexpressing ABA-responsive

complex (ABRC1) from the barley HVA22 showed improvedgrowth and yield in addition to enhanced tolerance againstcold, drought, and salt stress (71). Furthermore, AtERF11 wasshown to negatively modulate the ABA-mediated regulation ofethylene biosynthesis; furthermore, its overexpression con-ferred ABA hypersensitivity during post-germination growthunder stress conditions (72). ABA3/LOS5 encodes a Mo-cofac-tor sulfurase that catalyzes abscisic aldehyde to ABA conver-sion, and its constitutive expression in rice leads to significantlyhigher yield during drought stress under field conditions (73).Similarly, overexpression of MoCo sulfurase gene in soybeanresulted in enhanced biomass and yield along with improveddrought tolerance attributed to increased ABA accumulation,reduced water loss, and induced antioxidant enzymaticmachinery (74). Furthermore, 9-cis-epoxycarotenoid dioxyge-nase (NCED) has been shown to catalyze the conversion ofneoxanthin to xanthoxin. In addition, T-DNA insertionalnced3 mutants displayed impaired drought tolerance and lim-ited ABA accumulation under water stress, whereas tobaccoplants constitutively expressing NCED1 enhanced ABA accu-mulation in leaves, which leads to improved drought and salt

Figure 2. Complex transcriptional circuitry contributing toward secondary cell wall development in plants as influenced by abiotic stress. Thesecondary cell wall biosynthesis consists of two nodes: one is E2Fc-mediated and the other one is through the BR-signaling pathway. E2Fc is the masterregulator of downstream transcription factors that act in a coordinated manner to further result in synthesis, transport, and assembly of secondary cell wallcomponents such as cellulose, xylan, and lignin. Similarly, brassinosteroid signaling also modulates various downstream genes leading to cell wall remodelingunder stress as follows: BSK1 (BR-SIGNALING KINASE); BSU1 (BRI1 SUPPRESSOR1); BZR1 (BRASSINAZOLE-RESISTANT1); CAD4 (CINNAMYL ALCOHOL DEHYDRO-GENASE 4); CESA4/7 (CELLULOSE SYNTHASE 4/7); FLY1 (FLYING SAUCER 1); GSK2 (GSK3/SHAGGY-LIKE KINASES); GUX2 (UDP-GLUCURONATE: XYLAN �-GLUCU-RONOSYLTRANSFERASE 2); IRX7/9 (IROQUOIS HOMEOBOX 7); LAC4/17 (LACCASE 4/17); REV (REVOLUTA); SKP2A (S-PHASE KINASE-ASSOCIATED PROTEIN 2A);SND1/2/3 (STAPHYLOCOCCAL NUCLEASE AND TUDOR DOMAIN CONTAINING 1/2/3); VND 6/7 (VASCULAR-RELATED NAC DOMAIN 6/7); XTH (XYLOGLUCANTRANSFERASE/HYDROLASE); EXP (EXPANSINS). In this complex process, various NACs (NAM-ATAF1,2-CUC2) and MYBs act as the key master switches thatcontrol cell wall deposition.

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stress tolerance (75). Similarly, in tomato the constitutive over-expression of NCED1 displayed enhanced ABA accumulation,reduction in assimilation rates, leaf chlorosis, and higher bio-mass because of counteracting positive effects of ABA on leafexpansion and increased water status (76).

Similarly, BR pre-treated seeds demonstrated significantlyhigher accumulation of dry mass and antioxidant enzyme activ-ity in alfalfa under salt stress (77) and ameliorated growth andsurvival of Robinia pseudoacacia during water stress (78). Inaddition, BR application causes enhanced seedling growth insorghum under osmotic stress (79). Knockout T-DNA inser-tion mutant of Osgsk1 (a rice GSK3/SHAGGY-like proteinkinase gene, ortholog of AtBIN2/AtSK21, and negative regula-tor of BR signaling) depicted enhanced tolerance toward abioticstress, whereas OsGSK1 overexpression resulted in stuntedgrowth in Arabidopsis (80). In addition, hormones target vari-ous members of protein families playing a significant role ingrowth either individually or in a co-regulated manner,thereby indicating the synergistic action of metabolic path-ways (81). Biotechnological manipulation of these key pro-teins could allow not only the adaptation under adverse envi-ronmental conditions but also determine the flux inphytohormone biosynthesis for securing, in the long run,improved food production.

Future outlook

With the apparent changes in the global environment, agri-cultural production systems are liable to change. Thus, theremay be a need to produce cost-effective biomass to replace theexisting fossil fuel in the near future. At the same time, to ensureavailability of enough food for 9 billion people is indeed adaunting task. One possible solution to this challenge could beto make use of marginal lands with low input crops capable ofproviding high-biomass yield. Attempts are already being made

to modify the plant architecture in such a way that will led to“transgressive overyielding” of plant biomass. Furthermore,there are numerous options to explore plant–microbe interac-tions for enhanced biomass production in marginal and arablelands. It is noteworthy that most of these interactions are cur-rently unexplored, making it important to closely observe thesoil, the rhizosphere, and the endophyte populations. Engi-neered plants and their beneficial symbionts will pave the wayfor future strategies to modify them for higher biomass produc-tion to meet the demands of a growing population in a changingclimate scenario. Similarly, understanding how cellular differ-entiation occurs during cell wall development will provide deepinsight into designing cell wall architecture to enhance biomassunder environmental stresses. More importantly, identifyingthe key transcription factors directly regulating secondary cellwall biosynthesis genes will not only provide valuable clues tounderstand the evolution of secondary wall biosynthesis in vas-cular plants but also to uncover the complexity of the dynamicchanges during cell wall development and abiotic stressresponse. Similarly, the phytohormones have been found to beinvolved directly in plant responses to different stresses. How-ever, the identification and maintenance of optimal dose/re-sponse ratio of hormones still remain a tedious task, becausethe hormonal balance should be moderate to maintain homeo-stasis to provide abiotic stress tolerance and retain growth andbiomass. Much work has been done in the past decades on themolecular pathways modulating hormone biosynthesis and sig-naling and dissecting out their role in response to varied cli-matic conditions. Our Minireview will thus be fruitful in sug-gesting ways to genetically manipulate hormone biosynthesispathways for abiotic stress tolerance and for enhanced cropproductivity. In the future, it will be highly desirable to studythe response of plants toward a combination of stresses mim-icking the field conditions, as no stress ever comes alone!

Acknowledgment—We gratefully thank Professor Govindjee, Uni-versity of Illinois at Urbana-Champaign, for critical reading of themanuscript.

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Rohit Joshi, Sneh L. Singla-Pareek and Ashwani PareekEngineering abiotic stress response in plants for biomass production

doi: 10.1074/jbc.TM117.000232 originally published online January 16, 20182018, 293:5035-5043.J. Biol. Chem. 

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