Dynamics of cell wall structure and related genomic resources for drought tolerance in rice

Plant Cell Reports (2021) 40:437–459 https://doi.org/10.1007/s00299-020-02649-2 REVIEW Dynamics of cell wall structure and related genomic resources for drought tolerance in rice Showkat Ahmad Ganie1   · Golam Jalal Ahammed2  Received: 17 August 2020 / Accepted: December 2020 / Published online: January 2021 © The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature 2021 Abstract Key message  Cell wall plasticity plays a very crucial role in vegetative and reproductive development of rice under drought and is a highly potential trait forimproving rice yield under drought Abstract  Drought is a major constraint in rice (Oryza sativa L.) cultivation severely affecting all developmental stages, with the reproductive stage being the most sensitive Rice plants employ multiple strategies to cope with drought, in which modification in cell wall dynamics plays a crucial role Over the years, significant progress has been made in discovering the cell wall-specific genomic resources related to drought tolerance at vegetative and reproductive stages of rice However, questions remain about how the drought-induced changes in cell wall made by these genomic resources potentially influence the vegetative and reproductive development of rice The possibly major candidate genes underlying the function of quantitative trait loci directly or indirectly associated with the cell wall plasticization-mediated drought tolerance of rice might have a huge promise in dissecting the putative genomic regions associated with cell wall plasticity under drought Furthermore, engineering the drought tolerance of rice using cell wall-related genes from resurrection plants may have huge prospects for rice yield improvement Here, we review the comprehensive multidisciplinary analyses to unravel different components and mechanisms involved in drought-induced cell wall plasticity at vegetative and reproductive stages that could be targeted for improving rice yield under drought Keywords  Rice · Cell wall · Genomic resources · Drought · Vegetative growth · Reproductive growth · QTL · Resurrection plants Introduction Drought has remained one of the most prominent and persistent environmental issues severely affecting plant growth, development, and yield Information from the Global Drought Information System reveals that drought is becoming progressively severe and intense across the globe (Sircar Communicated by Wusheng Liu * Showkat Ahmad Ganie showkatmanzoorforever@gmail.com * Golam Jalal Ahammed ahammed@haust.edu.cn Department of Biotechnology, Visva-Bharati, Santiniketan, West Bengal 731235, India College of Horticulture and Plant Protection, Henan University of Science and Technology, Luoyang 471023, China and Parekh 2019) Rice (Oryza sativa L.) is one of the most important cereal crops feeding a large fraction of the human population worldwide (Ganie and Mondal 2015; Wang et al 2017; Xu et al 2018) To feed the rapidly expanding human population, the production of rice must be doubled by 2050 (Fischer et al 2009) However, this projected increase in rice production is restrained by several biotic and abiotic stresses (Song et al 2012; Li et al 2015a; Ganie et al 2017a; Kou et al 2017) Although rice is cultivated in diverse ecosystems ranging from flooded wetland to rainfed dryland, it is highly susceptible to drought due to shallow rooting behavior (Gornall et al 2010; Wang et al 2010; Xu et al 2018) The production of rice is highly water-intensive and is, therefore, grown under flooded conditions (Wang et al 2017; Xu et al 2019) Rice cultivation consumes almost 24–30% of the world’s available freshwater (Bahuguna et al 2018) Therefore, a water deficit in the form of drought can result in the huge yield losses of rice Almost 18 million tons of rice yield is lost globally per year due to drought (Dhakarey 13 Vol.:(0123456789) 438 et al 2017) The yield losses of rice are even more severe when periods of drought coincide with its sensitive growth stages (Kumar et al 2014) Different developmental growth stages of rice are affected by drought, with the flowering and grain-filling stages being the most drought-sensitive, resulting in severe yield penalties (Wang et al 2010; Bahuguna et al 2018) Under such circumstances, the development of high-yielding drought-tolerant rice varieties suitable for drought-prone areas is very crucial The prior sound knowledge of cellular and molecular mechanisms regulating the rice drought tolerance can accelerate the development of such varieties The primary and secondary cell walls differ in the arrangement, flexibility, and structure of matrix polymers, organization of microfibrils, rheological and mechanical properties, and their roles in the plant life (Cosgrove and Jarvis 2012) Primary walls, established during cell division in metabolically active and growing cells, are present in almost all plant cells, adequately flexible and hydrated to enable cell wall expansion during growth In contrast, the secondary cell walls are present only in differentiated tissues, synthesized once cell growth has stopped, laid inner to the primary wall, and characterized by lesser extensibility, more thickened walls with higher cellulose-content and mechanical strength, lesser hydration, and increased rigidity than primary walls (Novaković et al 2018) Despite these differences, the basic architecture of primary and secondary cell walls is the same, consisting of highly tensile cellulose fibers embedded in a physiologically active water-saturated matrix of non-cellulosic polysaccharides cross-linked with structural glycoproteins Whereas the cellulose microfibrils are ubiquitously present in all plant cell walls, the matrix composition of primary walls differs between different plant groups (Novaković et al 2018) In dicots, the matrix is composed mainly of xyloglucans and pectic polysaccharides in which the network of cellulose microfibrils are cross-linked with xyloglucans In contrast, the matrix in monocots has a high proportion of glucuronoarabinoxylans and (1 → 3), (1 → 4)-β-D-glucans that interact with cellulose microfibrils (Shivaraj et al 2018) Cellulose is the major constituent of cell walls which is synthesized by a large enzyme complex called cellulose synthase at the plasma membrane, and is composed of β-1,4linked glucan chains that are linked by hydrogen bonds to form high load-bearing cellulose microfibrils (Somerville et al 2004) For load-bearing, the cellulose fibrils crosslink with hemicelluloses and possibly also with pectins Hemicelluloses are highly branched polymers consisting of β-(1 → 4)-linked backbones that interact through extensive hydrogen bonding with cellulose fibers to reinforce their tensile strength (Cosgrove and Jarvis 2012) Xyloglucans and arabinoxylans are the most predominant hemicelluloses in plant cell walls (O’Neill and York 2018) Phenolic acids, 13 Plant Cell Reports (2021) 40:437–459 such as ferulic and p-coumaric acids can form cross-links between hemicellulose fibers to reduce the cell wall flexibility, which can affect the accessibility of wall modifying proteins (Sasidharan et al 2011) Pectins represent the most complex cell wall polysaccharides consisting of the basic building block galacturonic acid, which includes homogalacturonan (HG), xylogalacturonan (XGA), rhamnogalacturonan I (RGI), and rhamnogalacturonan II (RGII), with HG being the most abundant pectin (Shivaraj et al 2018) In the presence of C ­ a2+, the formation of hydrogel through crosslinking in de-esterified HG helps in load-bearing (Feng et al 2018) Besides C ­ a2+, the formation of pectin network also requires boron, which facilitates the cross-linking of RGII domains through boron-bridges (Chormova et al 2014) Pectins play a crucial role in the porosity, stiffness, mechanical strength, and adhesion of cell walls (Baldwin et al 2014) Besides the cellulose-hemicellulose and pectin networks, another network is constituted by carbohydrate-rich glycoproteins viz insoluble extensins (EXTs) and soluble arabinogalactan proteins (AGPs) in the cell wall The three networks are interlinked, and thus any alteration in the EXT/ AGP network can profoundly affect the cell wall structure leading to the biological consequences related to the cell wall (Nguema-Ona et al 2014) Cell wall metabolism is one of the crucial aspects of plant response to environmental stresses, which is mediated by various cell wall modifying proteins These proteins play crucial roles in modulating cell wall structure and properties, causing changes in cell enlargement and expansion during acclimation to such stresses (Sasidharan et al 2011) The interactions between cellulose microfibrils and hemicelluloses are modulated by three groups of enzymes: expansins (EXPs), xyloglucan endo-β-transglucosylase/hydrolases (XETs/XTHs), and endo-1,4-β-glucanases (EGases) which promote the cell wall extensibility (Sasidharan et al 2011) More specifically, the EXPs and XTHs facilitate the cell wall loosening by disrupting the hydrogen bonds between cellulose and xyloglucan polymers, whereas EGases so by catalyzing the endohydrolysis of 1,4-β-D-glucosidic bonds of cellulose (Bray 2004) XTHs also modulate cell wall extensibility through breaking and reforming of bonds between xyloglucan chains (Hyodo et al 2003) Pectins are acted upon by a group of cell wall modifying enzymes such as pectinmethylesterase (PME), pectate lyase (PL), and polygalacturonase (PG) to regulate the pectin stiffness, cell expansion, and growth (Bray 2004) PMEs modify cell walls by catalyzing demethylesterification of HGs to release acidic pectins (Micheli 2001) PMEs act on pectic polysaccharide domains either linearly, causing cell wall stiffening, or randomly promoting cell wall loosening, which is determined by the cellular pH and availability of ­Ca2+ (Micheli 2001) The de-esterified pectins released by PME action are then degraded by enzymes PL and PG to facilitate cell expansion Plant Cell Reports (2021) 40:437–459 through promoting cell wall loosening (Bray 2004) PL catalyzes eliminative cleavage of de-esterified pectin yielding oligosaccharides with unsaturated galacturonosyl groups at their non-reducing ends (Marín-Rodríguez et al 2002) In contrast, PG catalyzes the hydrolytic cleavage of HG regions in the middle lamella of the cell wall (Bray 2004) Another group of cell wall enzymes closely involved in cell wall loosening and stiffening is peroxidases These proteins promote either cell wall stiffening by facilitating bond formation through H ­ 2O2-mediated oxidation of aromatic cell wall compounds (monolignols, cinnamic acids, aromatic amino acids), or cell wall loosening by generating hydroxyl radicals which disrupt covalent bonding in cell wall polymers (Francoz et al 2015) The occurrence of the cell wall is one of the most important characteristics of plants allowing them to thrive in the terrestrial environment The cell wall is very crucial for providing shape and mechanical strength to withstand changing turgor pressures The cell wall is the frontline, where a plant cell comes in contact with various environmental stresses and, therefore, plays a pivotal role in mounting plant responses to such stresses (Hoson 2002) Concerted water uptake and irreversible cell wall expansion-driven cell enlargement are essential for optimal plant growth (Cosgrove and Li 1993) Drought reduces the growth and productivity of plants by causing various physiological changes, including loss of turgor (Le Gall et al 2015) Turgor pressure is a crucial factor in regulating cell growth, which is significantly governed by the extensibility of the cell wall (Wolf and Greiner 2012; Tardieu et al 2014) Drought-induced reduction in the cell turgor, therefore, decreases growth by decreasing cell expansion and/or elongation (Tardieu et al 2014) Morphological changes in plants under drought are profoundly governed by the modifications in the polysaccharide network of the cell wall Therefore, among the other mechanisms adopted by plants in response to drought, maintenance of tissue turgor via osmotic adjustment is very crucial for plant tolerance to drought Like other plants, it has been found that drought changes the cell wall properties in rice too (Dhakarey et al 2017; Li et al 2017; Hazman and Brown 2018; Bang et al 2019) Drought has been revealed to affect the tissue turgor leading to the reduced growth of rice plants (Farooq et al 2009a, b) Thus, drought may lead to rice growth inhibition by affecting its cell wall flexibility (Cal et al 2013) Due to the difficulty in analyzing cell wall dynamics, most of the studies on abiotic stress-induced modifications in the cell wall mainly focus on genes involved in the metabolism of the cell wall, rather than studying the precise nature of changes in the cell wall structure, composition, and properties (Tenhaken 2015) This difficulty may be due to the limited availability of imaging and biomechanical tools for studying the native cell walls, underuse of existing microscopy and NMR 439 methods in abiotic-stressed plants, stress-specific changes in the cell wall, and complications due to the crosstalk between stress and cell wall integrity signaling pathways (Rui and Dinneny 2020) Expression of several cell wall-related genes is regulated by drought in rice (Liu et al 2014; Tamiru et al 2015; Lee et al 2016; Jung et al 2017; Choi 2019) Therefore, in this article, we have comprehensively reviewed the role of different genomic resources in the metabolism of cell wall components for the vegetative and reproductive growth of rice under drought Furthermore, the potential of cell wall-related genes from resurrection plants in improving drought tolerance of rice is also discussed Drought‑responsive cell wall‑related candidate genes associated with vegetative growth of rice Plant phenology, leaf area, leaf surface properties, and root extension have been reported to act as the major constitutive traits mainly controlling water status in crop plants under drought (Bocco et al 2012; Wang et al 2016; Ahammed et al 2020) During the vegetative stage, upland and rainfed lowland rice is subjected to a varying degree of drought for different durations Drought during the vegetative growth of rice leads to its tissue death, leaf tip drying, leaf rolling, and stunted growth (Chang et al 1974; de Datta et al 1988; Li et al 2017; Islam et al 2018; Menge et al 2019) Besides, drought affects leaf area index, tillering capacity, shoot dry weight, and also the length, thickness, and depth of roots in rice (Bañoc et al 2000; Chu et al 2018; Hazman and Brown 2018) Evaluation of drought response at the vegetative stage of rice can be very beneficial for the early identification of desirable drought-tolerant genotypes for drought tolerance breeding (de Datta et al 1988) Remodeling of the cell wall in response to drought often causes changes in different aspects of the vegetative growth of rice, which are essential for drought tolerance (Fig. 1) Several drought-responsive genomic resources have been identified in rice, which are associated with the remodeling of the cell wall structure in different vegetative tissues and, therefore, with the dynamics of vegetative growth of rice under drought (Table 1) Root Drought avoidance is one of the elegant strategies adopted by plants for sustained growth and development in waterlimited conditions, and this is principally ascribed to root phenes that play a decisive role in water uptake and transport to the shoot system (Clark et al 2002; Lynch et al 2014) The root surface is where a plant first gets exposed to drought; therefore, the plasticity in root phenes under 13 440 Plant Cell Reports (2021) 40:437–459 Fig. 1  Cell wall plasticity-mediated growth of rice under drought Drought alters the expression of drought-responsive cell wall-related genes to promote the modifications in the cell wall structure This drought-induced cell wall plasticity modifies the different aspects of vegetative and reproductive growth of rice to withstand the harmful effects of drought Numerals indicate references for correspond- ing representative candidate genes involved in the different phenotypic aspects of vegetative and reproductive development: Todaka et  al (2012), Cal et  al (2013), Liang et  al (2018), Redillas et al (2012), Jung et al (2017), Ji et al (2005), 7, 8, 11 Vydehi (2007), Li et al (2015b), 10 Guo et al (2013) water-limited conditions plays a key role in coping with drought in cereal crops, including rice (Henry et al 2012; Kadam et al 2017) The elongation of the plant root system occurs as a result of cell division and cell expansion facilitated by the dynamic structure of the cell wall, which shows substantial expansion during the growth of root cells (Cano-Delgado et al 2000; Bassani et al 2004) Several genomic resources have been identified that are associated with the remodeling of cell wall structure for droughtinduced root elongation in rice (Table 1) Study of root proteome in drought-stressed JA-biosynthesis rice mutant cpm2 (having disrupted allene oxide cyclase gene) at the vegetative growth stage has revealed that the mutant had better root development in the form of profuse branching, increased length and more depth than wild-type plants (Dhakarey et al 2017) This root phenotype, for enhanced performance of cpm2 plants under drought, was supported by cell wall metabolite analysis of cpm2, where it was found that the contents of six major enzymes of phenylpropanoid pathway were increased, potentially modifying the cell wall 13 Roots Roots Roots Roots Stem nodes Roots OsERF71 OsERF48 OsNAC9 OsNAC10 OsPIL1 Cell wall composition OsCCR10 Unregulated Downregulated Upregulated Upregulated Upregulated Upregulated Upregulated Root, shoot OsTF1L Regulation Upregulated Tissue Vegetative growth Transcriptional regulation OsAP2 and OsWRKY24 Shoot Genes Functions Overexpression Lignin biosynthesis Overexpression Phytochrome-interacting transcription factor Overexpression TF Overexpression TF Overexpression TF regulating calcium signaling Overexpression TF regulating lignin synthesis Overexpression TF regulating lignin synthesis Overexpression TFs Approach Table 1  Drought-responsive cell wall dynamics-related genes of rice and their role in vegetative and reproductive growth of rice Decreases leaf rolling and wilting, increases survival rate, chlorophyll-content and photochemical efficiency Reduce plant and cell size Downregulate genes encoding EXPs and XETs/ XTHs Promotes shoot lignin accumulation and effective photosynthetic rate, reduces water loss Improves the root structure; elevates the expression of cell wall loosening and lignin biosynthetic (OsCCR1) genes Causes longer and dense root phenotype; regulates the expression of cell wall-related genes such as OsXTH9, OsAGP24 and OsAGP3 Improves the root architecture and photochemical efficiency; delays leaf rolling; upregulates OsCCR1 and wall-associated kinase genes Enlarges roots; reduces chlorophyll loss, leaf rolling and wilting; upregulates wall-associated kinase Causes dwarf phenotype by reducing cell elongation and internode length Downregulates expansins and cellulose synthase (Choi 2019) (Todaka et al 2012) (Jeong et al 2010) (Redillas et al 2012) (Jung et al 2017) (Lee et al 2016) (Bang et al 2019) (Jang and Li 2018) Effects on transgenic/mutant References plants Plant Cell Reports (2021) 40:437–459 441 13 13 Mutation Upregulated Upregulated OsARD4 Miscellaneous – – – – Downregulated Upregulated Upregulated Downregulated JA biosynthesis Cell wall loosening Cell wall loosening Cell wall loosening Cell wall biogenesis and modification Cell wall modification Cell wall stiffening Cell wall stiffening Overexpression Ethylene and polyamine biosynthesis – Roots Biosynthesis of non-cellulosic polysaccharides; regulation of cell cycle Functions Overexpression Degradation of pectin Upregulated Upregulated Mutation – – Young leaves Cell wall modification OsBURP16 Upregulated Approach Upregulated Upregulated in IR64; downregulated in Moroberekan Shoot apex, root tip SLE1 Regulation POD Roots Cinnamoyl-CoA reductase, Leaf elongation zone ferulate-5-hydroxylase, laccase, peroxidase, Myb52/54, Myb58/63 etc beta-1,3-glucanase and Leaf 3-glycosyl hydrolase OsEXP2 Seminal and lateral roots OsEXP2, XET, EGase Seminal root tips OsEXP2, EGase Seminal root tips Roots ENOD93, expansins, cell wall invertases Phytohormone biosynthesis AOC Roots Tissue Genes Table 1  (continued) (Yoshikawa et al 2013) Enhances branching, length and depth of roots; elevates the levels of six major enzymes of the phenylpropanoid pathway involved in cell wall remodeling Causes early initiation, profuse branching, more depth and high biomass of roots – – – – - (Ramanathan et al 2018) (Dhakarey et al 2017) (Yang et al 2004) (Yang et al 2003) (Zheng et al 2003) (Wang et al 2011) (Huang et al 2014) Decreases cell wall pectin- (Liu et al 2014) content and plant survival; increases electrolyte leakage, H2O2 accumulation and water loss of leaves – (Lin and Kao 2002) – (Cal et al 2013) Causes rolled- and narrowleaf phenotype; reduction in plant height; failure of cell-plate formation Effects on transgenic/mutant References plants 442 Plant Cell Reports (2021) 40:437–459 Roots Leaf, stem I12A1 MIR166 Upregulated Upregulated Upregulated Leaf, panicle Upregulated Upregulated Leaf OsDIS1 Upregulated Root tips at reproductive stage Leaf REL1 Downregulated Upregulated Upregulated Leaf CLD1/SRL1 Upregulated Regulation Roots at reproductive stage Anther Leaf OsDSS1 Reproductive growth Cell wall composition CesA10 OsAGP7, OsAGP16, OsAGP27, OsAGP30, OsAGP31 CSLA9, CSLC1, CSLC2, CSLE6 and XG-FTase Cell wall modification OsXET9 Tissue Genes Table 1  (continued) – – – – Cell wall loosening Cell wall biosynthesis Cellulose synthesis Constitute cell wall structure P450 monooxygenase Functions – – – – (Dong et al 2011) (Moumeni et al 2011) (Narciso et al 2010) (Ma and Zhao 2010) (Zhang et al 2018) (Nguyen et al 2004) (Ning et al 2011) (Liang et al 2018) (Li et al 2017) (Tamiru et al 2015) Effects on transgenic/mutant References plants Causes dwarf phenotype by reducing early seedling growth, plant height and internode length Alters expression of cell wall metabolism-related genes Causes severe leaf rolling Mutation Communication between and defect in cell wall the plasma membrane and formation; reduces cellucell wall lose- and lignin-contents; causes abnormal expression of cell wall-related genes Mutation – Causes leaf rolling and upregulates cell wallrelated genes Overexpression Ubiquitination Increases leaf rolling; alters the expression of cell wall development-related genes – Converts UDP-glucose to – UDP-galactose Knockdown Regulates the expression of Causes leaf rolling; reduces class III HD-Zip TFs transpiration rate and diameter of xylem vessels; expression of OsHB4 TF is upregulated which in turn regulates the expression of the cell wall and polysaccharide synthesisrelated genes Mutation Approach Plant Cell Reports (2021) 40:437–459 443 13 Spikelet Anthers Anthers, pistils Florets Peduncle base Sucrose metabolism SuSy, CWI OsCIN4 INV4 INV2 OsCIN2 (Bahuguna et al 2018) (Nguyen et al 2010) (Li et al 2015b, a) (Jin et al 2013) (Ji et al 2005) Upregulated Anther OsDIL Upregulated Downregulated Upregulated Downregulated Upregulated – – – – – Sucrose metabolism Sucrose catabolism Sucrose catabolism Sucrose catabolism Sucrose catabolism – – – – – Pectin-binding receptor-like Causes anther indehiscence, (Vydehi 2007) kinase reduced pollen viability and dwarf phenotype; affects root development (Guo et al 2013) Overexpression Formation of water-proof Protects the pollen and lipid barriers anther cell walls from drought Gene silencing Downregulated Cell wall loosening Cell wall extension – – – – Downregulated Downregulated β-expansin Florets Cellulose synthase, cell wall Young panicles invertase, laccase and glycoside hydrolase OsiWAK1 Roots at reproductive-stage Functions Approach Regulation Tissue Genes Table 1  (continued) 13 (Jin et al 2013) (Wang et al 2011) Plant Cell Reports (2021) 40:437–459 Effects on transgenic/mutant References plants 444 composition by altering the levels of cell wall biopolymerlinked coumaric and ferulic acid These results suggest that the deficiency of jasmonic acid (JA) can stimulate cell wall adaptations in the roots of rice during drought, and that JA is a negative regulator of root growth and drought response in rice Genes in the AP2/ERF transcription factor (TF) family regulate various developmental and physiological processes related to the responses of rice to various abiotic stresses (Nakano et al 2006; Ganie et al 2019) Functional characterization of a drought inducible AP2/ERF family TF gene OsERF48 has revealed that its overexpression leads to the longer and dense root phenotype in transgenic plants (Jung et al 2017) The study also showed that this TF regulated the expression of a series of target genes, including cell wallrelated genes such as OsXTH9, OsAGP24, and OsAGP3, which might be involved in the drought-induced altered root phenotype These target genes of OsERF48 encode XTH and AGPs, which are reported to be associated with cell expansion and cell wall plasticization-mediated root growth under abiotic stress conditions (Yang et al 2006; Seifert and Roberts 2007) Overexpression of another AP2/ERF type gene OsERF71 in the rice roots has been found to elevate the expression of cell wall loosening and lignin biosynthetic genes (EXP, XTH, OsCCR1, OsCCR10, OsCAD, OsC4H), which modify the root structure and, therefore, confer drought resistance phenotype at the vegetative stage of rice growth (Lee et al 2016) The root-specific overexpression of the same TF gene was later found to enhance the drought tolerance of rice shoots by increasing their photochemical efficiency under drought (Lee et al 2017a) Although authors provided no evidence for developmental changes, they assume that this increase in the shoot drought tolerance may be due to the modification in the shoot developmental processes such as leaf growth inhibition, leaf water content, and leaf cell wall hardening The NAC (NAM, ATAF, and CUC) group of TFs are among the most extensively studied candidates for improving drought tolerance in plants Several NAC genes involved in drought tolerance of rice have been reported (Hu et al 2006; Nakashima et al 2007; Zheng et al 2009; Jeong et al 2010; Redillas et al 2012 etc.); however, only a few of them are involved in drought response by modifying the rice cell wall structure Rice plants overexpressing OsNAC9 have been shown to exhibit the altered root architecture in the form of the profoundly enlarged stele and aerenchyma at the vegetative stage of growth under drought conditions (Redillas et al 2012) This root phenotype was attributed to the significantly upregulated genes, including wall-associated kinases (regulating cell elongation and morphogenesis) and lignin biosynthetic gene OsCCR1 The NAC gene OsNAC10 has been reported to confer drought tolerance to rice by increasing the root diameter at the vegetative stage in almost the same way as in the case of OsNAC9 (Jeong et al 2010) Enlarged root Plant Cell Reports (2021) 40:437–459 cortical aerenchyma improves drought tolerance by diminishing the metabolic costs of the root, which facilitate root growth and water-uptake from water-limited soil (Redillas et al 2012); whereas, the increased root diameter results in drought resistance by encouraging the root penetration in the soil (Clark et al 2008) Another rice NAC gene OsNAC6 has been reported to orchestrate root structural adaptations in the form of increased root number and root diameter for enhancing drought tolerance (Lee et al 2017b) However, the authors have not reported whether OsNAC6 does so by remodeling the cell wall structure Together, these results indicate that rice ERF and NAC TFs recruit factors associated with cell wall modification to facilitate root morphological adaptations in response to rhizosphere drought Moreover, a lignin biosynthesis gene OsCCR10 (Oryza sativa CINNAMOYL-COA REDUCTASE 10) is highly induced by drought in the roots of rice (Choi 2019) The study showed that the overexpression of this gene enhances the drought tolerance of rice by decreasing the extent of leaf rolling as well as wilting, and also by increasing the survival rate, chlorophyll-content, and photochemical efficiency In order to elucidate the possible molecular mechanisms regulating crop development under environmental stresses, transcriptomic methods such as microarray, RNA-seq, and cDNA-amplified fragment length polymorphism (AFLP) have been widely used to identify the stress-responsive differentially expressed genes Besides the functional characterization of some cell wall-specific genes for droughtinduced root plasticity, as mentioned above, several other cell wall-related genes have been identified to be differentially expressed in different types of root tissues of rice under drought conditions by using transcriptomic methods In a transcriptomic study, water deficit has been reported to repress the expression of an expansin gene OsEXP2 in the seminal and lateral roots, where growth is generally stimulated under water-limited conditions; whereas, its expression was found to be upregulated in the adventitious roots (Yang et al 2004) This distinctive expression of OsEXP2 indicates that this gene may be linked to primary root growth However, a separate transcriptomic study found that OsEXP2, along with two other cell wall loosening genes XET and EGase, was rapidly upregulated in the seminal root tips during root elongation of rice in response to water-limited conditions (Yang et al 2003) The contrast in the expression of OsEXP2 in the two studies is anomalous, because both studies employed cDNA-AFLP to profile gene expression in upland rice variety Azucena High expression of OsEXP2, XET, and EGase, under water-limited conditions possibly facilitates the extensibility of cell walls ensuing in cell expansion in the elongation zone, thus stimulating root elongation (Wu and Cosgrove 2000; Lee et al 2001) Besides, identification and differential expression of 17 cell wall-related genes have been reported in the elongation 445 zone of water-stressed rice roots (Yang et al 2006) Out of the 17 genes, five genes were found to be associated with cell wall loosening (OsEXP1, OsEXP2, EGase, and two XETs), six genes with lignin biosynthesis (PAL, C3H, 4CL, CCoAOMT, CAD, and peroxidase), and the six other genes with the metabolism of cell wall proteins (GRP and UDP-GlcNAc pyrophosphorylase) and polysaccharides (OsCslF2, GMPase, xylose isomerase, and beta-1,3-glucanase) The four polysaccharide metabolism-related genes encode enzymes that catalyze the synthesis of hemicellulose, hydrolysis and synthesis of β-glucan cross-links in cell wall polysaccharides, and activation of mannosyl units for cell wall synthesis A south Indian deep-rooted rice landrace, Nootripathu, is an efficient drought-avoider, maintaining its root growth under severe drought (Babu et al 2001) To decipher the molecular and biochemical bases of high drought tolerance in Nootripathu, comparative droughtresponsive transcriptome profiling has been performed on the roots of this landrace and shallow-rooted droughtsensitive rice variety IR20 (Muthurajan et al 2018) The results revealed significant upregulation of cell wall-related genes cellulose synthases, endoglucanases, and expansins in the roots of Nootripathu as compared to IR20 (Muthurajan et al 2018) The upregulation of these genes might be associated with cell wall loosening leading to the accelerated root growth in Nootripathu under drought conditions In a separate transcriptome analysis, the cell wall biogenesis and modifying genes such as those encoding ENOD93 proteins, expansins, and cell wall invertases, were found to be significantly downregulated in the roots of drought-tolerant rice line DK151 (Wang et al 2011) Although these genes are usually upregulated in drought-tolerant genotypes under water-limited conditions, the authors justify their results by speculating that inhibition of cell wall extension (by downregulation of the corresponding genes) in root tissue under drought is an economic process saving energy for the sustenance of rice plants under drought conditions Cell wall peroxidases are involved in the reduction of cell growth by causing the stiffening of cell walls (Fry 1986) Osmotic stress-induced inhibition of root growth in seedlings of rice has been reported to be due to high activity of cell wall peroxidase, which catalyzes the cell wall stiffening process by forming the cross-links between cell wall polymers (Lin and Kao 2002) Functional analysis of these cell wall-related droughtresponsive genes identified in the different types of root tissues of rice may pave the way towards understanding the molecular mechanisms underlying the regulation of cell wall plasticization-mediated root growth in rice under limitedwater conditions 13 446 Shoot Although root is the frontline organ, where a plant encounters drought, research on leaves is equally important, because leaves are the source organs that synthesize assimilates for the sink organs to sustain the growth of the whole plant even during the stress conditions It is also known that drought affects foliar plant parts more directly than roots in rice (Farooq et al 2009a, b) Besides, through some cell wall plasticization-mediated adaptive mechanisms, leaves also play a crucial role in reducing water loss during the periods of water scarcity (Cal et al 2013) One of the important symptoms of drought in plants is the rolling of leaves, and it is deemed as an agronomically important trait in rice breeding Leaf rolling phenotype is partly regulated by the formation of specific thin-walled and highly vacuolated cells called bulliform cells, which are present on the adaxial surface of leaves (Fang et al 2012; Xiang et al 2012; Li et al 2017) These specific cell types lose turgor under water stress, resulting in leaf rolling phenotype (Price et al 1997; Fang et al 2012) Moderate leaf rolling in rice and other field-grown crops helps in attaining the erect architecture of leaves, facilitating the enhanced light capture and gas exchange for efficient photosynthesis, which results in the accumulation of dry matter and increased yield (Zhu et al 2001; Lang et al 2004) However, severe leaf rolling has detrimental effects on plant growth, development, and grain yield (Li et al 2017) Since moderate leaf rolling diminishes the water loss by reducing the transpiration rate, it can facilitate the survival of plants under drought (Kadioglu et al 2012; Liang et al 2018) Hence, the manipulation of leaf rolling can prove as one of the most vital approaches towards enhancing rice productivity under drought (Zou et al 2011) Keeping its agronomic importance in view, leaf rolling has greatly attracted the attention of plant scientists, and consequently, many different types of genes, and molecular mechanisms underlying the regulation of leaf rolling in rice have been studied (Zhang et al 2009; Li et al 2010; Zou et al 2011; Xiang et al 2012; Yang et al 2014) However, only a few of them have been reported to be involved in droughtinduced leaf rolling in rice by modifying the cell wall structure Functional characterization of a gene Curled Leaf and Dwarf 1/Semi-Rolled Leaf (CLD1/SRL1), encoding a glycophosphatidylinositol (GPI)-anchored membrane protein, has revealed that it is involved in leaf rolling-mediated drought tolerance in rice by regulating the cell wall formation and leaf epidermal integrity (Li et al 2017) The study found that the leaves of cld1 mutant exhibited a defect in cell wall formation due to the significantly reduced celluloseand lignin-contents, which in turn owes to the abnormal expression of cell wall-related genes (OsCESA1-3, SND1, OsDRP2B, etc.) and proteins (OsCAD2, Os4CL3, laccase, OsCesA8, OsXTH8, etc.) The study also maintains that 13 Plant Cell Reports (2021) 40:437–459 the defect in epidermal bulliform cells in the leaves of the cld1 mutant leads to severe leaf rolling, which causes reductions in the water-retaining capacity and water potential in leaves, resulting in the reduced drought tolerance Leaf rolling and erectness is also regulated by REL1 (Rolled and Erect Leaf 1) gene in rice (Chen et al 2015) A dominant mutation in this gene (rel1-D) has been reported to result in the high drought tolerance in rice due to the significant upregulation of different types of genes, including droughtresponsive, ABA-responsive, superoxide dismutase, and cell wall-related genes (LOC_Os01g64860; LOC_Os01g72510; LOC_Os05g35320; LOC_Os12g36810, etc.), implying that REL1 is a negative regulator of drought tolerance in rice (Liang et al 2018) The study proposes that rel1-D-mediated leaf rolling and drought tolerance in rice is caused by the perturbed dynamics of stress response in specific organelles such as cell wall and vacuole In another study, overexpression of an E3 ubiquitin ligase gene OsDIS1 (Oryza sativa drought-induced SINA protein 1) has been shown to decrease the drought tolerance in rice by increasing the leaf rolling and by affecting the expression of a wide range of genes, including those involved in drought response and in cell wall development (Ning et al 2011), indicating that OsDIS1 has a negative role in regulating drought tolerance in rice Mutation of SLE1 (Slender Leaf 1) gene, encoding a cellulose synthase D4-like enzyme that is potentially involved in cell plate formation, in rice leads to a distinct rolled- and narrow-leaf phenotype, besides other pleiotropic developmental abnormalities (Yoshikawa et al 2013) Although the authors presume that the impaired root development could cause the drought stress in sle1 mutants, it is also possible that the mutants might as well have experienced drought due to the severely rolled- and narrow-leaf phenotype A 2OG-Fe (II) oxygenase-encoding gene RL14 (Rolling Leaf 14) has been shown to regulate the leaf rolling and water transport by altering the expression of cellulose and lignin biosynthetic genes (SND1, VND4/5/6, MYB58/63, MYB20, OSLAC4, OSLAC17, OSCEA4), and hence, the secondary cell wall composition in rice leaves (Fang et al 2012) The rl14 mutant rice plants were found to have water deficiencytriggered shrunk bulliform cells and reduced transpiration rate Although these morpho-physiological features are associated with drought tolerance, the authors have not specifically reported the drought-responsive role of RL14 in rice; hence, keeping an avenue open for characterization of RL14 as a drought-responsive gene in rice In a similar study, a NAC family gene OsSND2 has been identified to regulate leaf rolling and cell wall biosynthesis by increasing cellulose-content in rice (Ye et al 2018); however, authors have not mentioned whether it can so under drought conditions as well MicroRNAs (miRNAs) are non-protein coding RNAs that regulate diverse developmental and stress-response Plant Cell Reports (2021) 40:437–459 processes, and thus miRNAs are regarded as critical genomic resources modulating agronomic traits in crop plants (Ganie et al 2016, 2017b; Li and Zhang 2016; Shriram et al 2016) In monocots, whether a leaf is rolled or flat is also determined by the antagonistic expression patterns of small RNAs and their target transcription factors on the adaxial and abaxial surface of the leaf (Moon and Hake 2011; Merelo et al 2016) In rice, OsHB4 (belonging to homeodomainzip III family of TFs) has been identified as a major target gene of miR166, and Short Tandem Target Mimic systemmediated knockdown of miR166 has been demonstrated to confer drought tolerance by causing morpho-physiological changes such as leaf rolling (due to small bulliform cells), reduced transpiration rate and decreased diameter of xylem vessels (Zhang et al 2018) Furthermore, in the knockdown rice lines, the study has also identified the downstream genes of the miR166-OsHB4 module which are related to cell wall formation and polysaccharide synthesis, such as CSLA3, CESA5, CSLF6 and CLAVATA1; and these genes were found to be strongly enriched among the differentially expressed genes Overall, these results imply that miR166 regulates the expression of OsHB4, which in turn regulates the expression of some cell wall and polysaccharide synthesis-related genes to modulate the cell wall structure for drought-induced morphological and developmental plasticity in rice Besides, functional analysis of drought-responsive miRNA regulatory networks has revealed miRNA-target genes involved in cell wall metabolism in rice (Chen and Li 2018) The characterization of these miRNA-target modules can, therefore, be useful for getting insights into the drought-induced metabolism of the cell wall in rice PG, a cell wall hydrolase, is responsible for the degradation of pectin in the cell wall (Swain et al 2011) Overexpression of a drought-inducible gene OsBURP16 (encoding β subunit of PG1) enhanced the sensitivity of rice to drought by decreasing plant survival rate and increasing the electrolyte leakage, H ­ 2O2 accumulation, and water loss rate of leaves (Liu et al 2014) The increased expression of OsBURP16 was, therefore, suggested to decrease the cell wall pectin-content, which affected the cell wall integrity and transpiration rate, resulting in increased sensitivity to different abiotic stresses, including drought (Liu et al 2014) Lignin is another essential constituent of the cell wall, which strengthens the plant stiffness Plants modify their cell wall structure in response to drought by accumulating high levels of lignin (Hu et al 2009; Bang et al 2019) The hydrophobic property of lignin prevents water loss from plant tissues under water-limiting conditions (Lee et al 2017a) A gene, encoding homeodomain-leucine zipper transcription factor OsTF1L, has been reported to be a key regulator of droughtinduced lignin accumulation in rice (Bang et al 2019) Overexpression of this gene in rice was shown to significantly increase the drought tolerance at the vegetative stage by 447 promoting shoot lignin accumulation and effective photosynthetic rate with a concomitant reduction in water loss (Bang et al 2019) The study also maintains that elevated lignin accumulation in transgenic rice plants occurred due to the upregulation of a series of lignin biosynthetic genes It has been elucidated that besides hormone action, abnormalities in the cell wall structure, deposition, and remodeling can result in plant dwarfism by affecting cell elongation or cell size (Reiter 2002; Zhou et al 2006) Mutation in a droughtresponsive cytochrome P450 gene OsDSS1 (Oryza sativa Dwarf and Small Seed 1) causes dwarf phenotype in rice by reducing the early seedling growth, mature plant height and internode length (Tamiru et al 2015) Since the expression of cell wall metabolism-related genes (OsBgal2, OsCESA1, OsEXP3, OsEXP4, and OsGLU1) was affected in the dss1 mutant, the authors relate the dwarfism to the altered cell size A similar study provided an excellent model for regulation of rice plant height via cell wall biosynthesis and development under drought (Todaka et al 2012) The study reported that a phytochrome-interacting factor (PIF)-like gene OsPIL1 acts as a negative internodal growth regulator in rice under drought, resulting in the dwarf phenotype The authors ascribe this role of OsPIL1 to the inhibition of cell elongation via down-regulation of its target genes (expansins and cellulose synthase), which are involved in the dynamics of the cell wall structure It can be deduced from these two studies that adopting a dwarf phenotype under drought conditions may be a crucial morphological adaptation to drought in rice Overexpression of two drought-responsive TF genes OsAP2 and OsWRKY24 has been found to reduce the plant and cell size in transgenic Arabidopsis, which could be due to the decreased expression of some genes encoding EXPs andXTHs—the genes associated with cell elongation through cell wall loosening (Jang and Li 2018) On the contrary, these two TF genes were earlier found to be positive regulators of cell elongation in rice (Jang and Li 2017), which indicates that these TFs regulate a different set of downstream target genes in monocots and dicots Germins and Germin-like proteins (GLPs) play important roles in the tolerance of plants to biotic and abiotic stresses (Ilyas et al 2016) Functional characterization of the promoter of OsRGLP1 revealed that it is highly induced by drought and that its activity is very high in cell walls besides other cellular components (Ilyas et al 2019) The cell wall-specific activity of the OsRGLP1 promoter suggests its possible role in strengthening the cell wall—a prominent mechanism for combating environmental stresses Furthermore, an effective response of plants to drought depends largely, besides other processes, on efficient adjustment of carbohydrate metabolism and source-sink relationships among different organs (Stitt et al 2007; Figueroa and Lunn 2016) It has been found that under drought, source organs (mature leaves) have lower sucrose and starch concentrations but higher hexose 13 448 concentration than sink organs (roots and immature leaves) (Luquet et al 2008), which indicates that drought reduces the availability of soluble hexoses (glucose and fructose) to sink organs resulting in decreased growth However, the higher concentration of sucrose in the sink might act as a signal for the upregulation of cell wall invertase genes OsCINs, which metabolize the sucrose into hexoses for maintenance of the sink activity, i.e., growth of the shoots and leaves, under drought (Luquet et al 2008) Besides the transcriptomic studies on root tissues, there are also a few transcriptomic profiling studies that have identified some other cell wall-related genes and reported their differential expression in different types of shoot tissues of rice under drought conditions Analysis of global gene expression profile in the leaf elongation zone of two contrasting rice cultivars, differing in leaf elongation rate, under drought has shown that an opposite regulation of cell wall dynamics occurs in the two genotypes, which might be causing differences in their leaf elongation under soil water deficit (Cal et al 2013) Most of the cell wall-related genes (e.g., cinnamoyl-CoA reductase, ferulate-5-hydroxylase, laccase, peroxidase, Myb52/54, Myb58/63 etc.) identified were found to be associated with the secondary cell wall deposition, lignification, and lignin polymerization leading to the less extensible cell walls These genes were found to be downregulated in the drought-tolerant Moroberekan but upregulated in sensitive cultivar IR64, signifying that the higher expression of these genes ceases or reduces the leaf elongation in the sensitive cultivar under mild drought A transcriptomic profiling study on the drought-stressed leaf samples of two rice genotypes with disparate sensitivities to drought revealed that many genes associated with cell wall metabolism were enriched only in the case of droughttolerant rice genotype (Baldoni et al 2016) These genes were associated with growth-regulating processes of lignin polymerization, peroxidation, xyloglucan modification, and secondary cell wall deposition, indicating the presence of alternative strategies in the drought-tolerant and sensitive rice genotypes for regulating leaf elongation under drought In another study, investigation of transcriptome differences between a drought tolerant introgression line (H471) and its sensitive recurrent parent (HHZ) using deep transcriptome sequencing has revealed a distinct global transcriptome reprogramming in the leaf samples of two rice genotypes under drought (Huang et al 2014) The authors found that among many genes that were differentially regulated between the two genotypes, cell wall modifying genes beta1,3-glucanase and family glycosyl hydrolase were found to be significantly up-regulated in H471 as compared to HHZ, indicating that high expression of these cell wall-related genes might be facilitating the physiological and metabolic adaptation of H471 to drought 13 Plant Cell Reports (2021) 40:437–459 Additionally, a proteomic study on rice cell wall under dehydration stress has identified several novel proteins related to the cell wall metabolism, such as S-adenosylmethionine synthetase or methyltransferase, adenosine kinase, S-adenosyl-L-homocysteine hydrolase, polygalacturonase, etc (Pandey et al 2010) Functional analysis of these drought-responsive cell wallrelated genes identified in the different types of shoot tissues of rice may facilitate the targeted engineering of cell wallspecific metabolic routes in the shoot system for improving drought tolerance in rice Drought‑responsive cell wall‑related candidate genes associated with reproductive growth of rice The sensitivity of rice to drought is the most acute during reproductive development, especially during flowering, which leads to severe yield loss (Li et al 2015b) The yield loss in rice is considerably more severe when periods of drought coincide with reproductive growth than that occurring during the vegetative growth (Wang et al 2010; Jin et al 2013) Even if the drought occurs at the tillering stage of vegetative development, it affects the reproductive growth of rice by reducing the number of reproductive tillers and panicles per hill (Wopereis et al 1996) Besides, the yield loss of rice (due to reproductive phase drought) can be attributed to the adverse effects of drought on different aspects of reproductive growth such as pollen cell function, spikelet fertility, seed set, and maturation of newly formed seeds (Liu and Bennett 2011; He and Serraj 2012; Guo et al 2013) Despite knowing the importance of reproductive growth for rice yield plus the highly adverse effects of drought on the reproductive development of rice, there is still a significant knowledge gap in the mechanistic understanding of molecular mechanisms and metabolic pathways involved in regulating the responses of rice to drought during reproductive growth As compared to the vegetative growth, there is a critical deficiency of studies involving comprehensive functional characterization of different types of genomic resources regulating the reproductive growth of rice under drought Notably, the studies about the functional characterization of cell wall-related genomic resources associated with the dynamics of reproductive growth of rice under drought are almost lacking To our belief, studies (except Guo et al (2013) and Vydehi (2007)) that have reported the identification of drought-responsive cell wall-related genes for reproductive growth of rice are mostly based on transcriptome analyses (Table 1), which are reviewed as follows Drought-induced altered expression of various cell wall dynamics-related genes at the reproductive stage of rice is essential for its reproductive success during the conditions Plant Cell Reports (2021) 40:437–459 of drought (Fig. 1) Lipid transfer proteins (LTPs) are smallsized, compact, heat-insensitive proteins that bind and transport different types of lipids (Lindorff-Larsen and Winther 2001; Cheng et al 2004; Edqvist et al 2018) LTPs are essential for the deposition of lipid monomers, which assemble water-proof lipid barriers on plant surfaces in the form of the cuticle, suberin, and sporopollenin (Edstam et al 2013) Some LTPs are important for plant growth because of their involvement in cell wall loosening activities (Nieuwland et al 2005) Besides, LTPs could also be involved in reducing drought-induced water loss by strengthening the cell wall (Sterk et al 1991; Guo et al 2013) Altogether, these findings suggest that LTPs can be involved in plant growth by altering the cell wall structure under drought Overexpression of an LTP gene OsDIL (Oryza sativa Drought-Induced LTP) has been found to enhance the drought tolerance during the reproductive growth of rice (Guo et al 2013) The authors suggest that OsDIL might protect the pollen and anther cell walls from drought by facilitating the synthesis of anther cuticle and pollen exine, which leads to the improved reproductive performance of transgenic plants under drought Wall-associated kinases (WAKs) belong to the receptor-like kinase gene family, which contribute to the maintenance of cell wall integrity in planta (Engelsdorf and Hamann, 2014) WAKs bind to pectin in the cell wall in response to abiotic stresses, and the WAK genes have been reported to be upregulated in plants displaying tolerance to abiotic stresses (Kohorn et al 2012; Le Gall et al 2015) WAKs are reportedly involved in cell elongation (Wagner and Kohorn, 2001), perhaps due to their role in cell wall modulation Expression of a WAK gene OsiWAK1 has been found to be downregulated under drought in rice roots (Vydehi 2007) Furthermore, OsiWAK1 was functionally characterized, whereby it was found that the silencing of this gene led to the severely affected root development and dwarf phenotype in rice (Vydehi 2007) Besides, the silenced plants were also found to exhibit anther indehiscence and reduced pollen viability, causing a sterility phenotype Given the relatively large number of WAK genes in rice (125 members) and their diverse roles in plant biology (Kanneganti and Gupta 2008), it remains a significant challenge to uncover their roles in the development of rice under drought Although there is feeble progress in functional analysis of cell wall-related drought-responsive genes for the process of reproductive growth of rice, many gene expression studies conducted on the reproductive growth of rice have identified differentially expressed genes associated with the dynamics of cell wall under drought For example, a gene expression profiling study at booting and heading stages of rice reproductive development under different abiotic stresses, including drought, has led to the identification of a highly upregulated gene OsXET9, which codes for a cell 449 wall xyloglucan endotransglucosylase (Dong et al 2011), indicating that this gene may play a role in the metabolism of the cell wall for promoting reproductive growth of rice under drought As already mentioned, xyloglucan endotransglucosylase genes are associated with cell elongation through cell wall loosening (Jang and Li 2018) AGPs are highly glycosylated proteins which are basal components of the cell wall, and these proteins are reported to be associated with regulation of cell wall plasticization-mediated plant growth under abiotic stress conditions (Yang et al 2006; Seifert and Roberts 2007; Schultz et al 2002) Expression analysis of AGP gene family in rice has revealed that several members of this gene family exhibit a predominant antherspecific expression and also show differential expression under drought (Ma and Zhao 2010), implying that these genes might have important roles to play in the reproductive growth of rice under water-limited conditions The authors propose that oligosaccharides, generated by the deglycosylation of polysaccharide chains of AGPs, might reduce the dehydration rate by elevating the intracellular osmotic pressure under drought Cell wall plasticity-mediated cell expansion is essential for the growth of roots during drought, requiring coordination among many different types of cellular processes (Dolan and Davies 2004) In this connection, a gene expression study has been performed to elucidate the drought-induced expression patterns in root tips of droughttolerant and susceptible rice genotypes at the reproductive stage (Moumeni et al 2011) The study found that among the other genes, expression of cell wall biosynthesis genes (such as CSLA9, CSLC1, CSLC2, CSLE6 and XG-FTase) was specifically upregulated in drought-tolerant genotypes under severe drought These results imply that the upregulation of these cell wall biosynthetic genes might promote the growth and elongation of roots in drought-tolerant rice genotypes for efficient water uptake to support their reproductive growth It also suggests that the promotion of root growth might support the reproductive growth of rice under drought Another expression profiling study for drought responsiveness in rice has found that several genes for cell wall extension are exclusively repressed in young panicles, such as genes encoding for cellulose synthase, cell wall invertase, laccase, and glycoside hydrolase (Wang et al 2011) The repression of these genes in young panicles under drought indicates their involvement in panicle development of rice under the conditions of drought The synthesis of sugars during photosynthesis and their subsequent metabolism by specific transporters and invertases (vacuolar and cell wall invertases) are very important processes for the normal development and viability of reproductive organs (Li et al 2015b) Invertases play an important role in strengthening sink tissues (e.g., anthers) by facilitating the unloading of sucrose from phloem and catabolizing the disaccharide into fructose and glucose to 13 450 be used as a source of energy in sink cells (Weschke et al 2003; Wang and Ruan 2012) Accordingly, any impairment in the activities of vacuolar and cell wall acid invertases can cause accumulation of sucrose, leading to sugar starvation-mediated energy shortages and sterility in developing anthers (Saini and Westgate 2000; Oliver et al 2005) Drought-induced reactive oxygen species (ROS) production and programmed cell death (PCD) activation have been demonstrated to cause male sterility in the anthers of a drought-sensitive rice cultivar (Nguyen et al 2010) This sterile phenotype was suggested to be associated with the downregulation of cell wall invertase OsCIN4 in the anthers, which might have blocked the sugar supply to the developing microspores, leading to excessive ROS production and ATP depletion due to the inactivity of the tri-carboxylic acid cycle in the mitochondria of microspore cells Another study proposed the involvement of OsCIN4 (as INV4 in that study) in the development of rice anthers under drought conditions (Li et al 2015b), indicating that this gene is tightly associated with the rice reproductive development and yield under water-limited conditions In that study, quantification of temporal metabolomic and transcriptomic changes in floral organs under combined drought and heat stress in two contrasting rice cultivars was performed, which revealed that sugar metabolism is a crucial component differentiating the responses of floral organs to these stresses (Li et al 2015b) The study found that expression of MST8 (encoding an anther-specific sugar transporter) and INV4 (encoding a cell wall invertase) was highly upregulated in the anthers of drought-tolerant genotype N22 Since these two genes act as markers for sink strength in the anthers of rice (Oliver et al 2005, 2007), the results indicate that N22 averts reproductive failure under heat and drought by avoiding carbohydrate starvation in its anthers Similarly, a separate study found that drought-induced male sterility in drought-sensitive rice cultivar Nipponbare is correlated with the downregulated carbohydrate metabolism (Jin et al 2013) The study found that cell wall invertase gene INV2 was significantly downregulated in the drought-stressed rice florets, indicating that INV2 might also be involved in the sugar unloading in the anthers under drought and that drought-induced repression of this gene might also contribute to sugar starvationmediated male sterility in rice The study also found that a β-expansin gene (Os03g0106500), which regulates cell wall dynamics and cell size in rice (Suwabe et al 2008), was also significantly repressed in the drought-stressed florets This indicates that impairment in microspore cell wall formation might also contribute to the male sterility under drought Drought has been found to adversely affect panicle (head) exsertion and anthesis in rice (O’Toole and Namuco 1983; Muthurajan et al 2011) It is also known that cell wall invertases are actively involved in the development of new sink tissues by allocating carbon to them 13 Plant Cell Reports (2021) 40:437–459 (Weschke et al 2003) Taking these points into account, Ji et al (2005) examined the tissue-specific expression of cell wall invertase genes of rice (OsCIN1-9) at the flowering stage under drought and found that these genes showed varied expression in flag leaves, panicles, anthers, and peduncles Particularly, the authors found that OsCIN2 showed a strong expression specific to the peduncle base Since panicle exsertion is caused by elongation of the peduncle (Ji et al 2005; Muthurajan et al 2011), OsCIN2 might play a crucial role in the heading of rice under drought Apart from these studies, cell wall invertases have also been found to be involved in drought priming-mediated acclimation of rice to drought (Bahuguna et al 2018) Drought priming is an elegant strategy to reduce the severity of terminal drought in plants (Harb et al 2010; Wang et al 2015) Priming with mild drought before flowering has also been found to boost the acclimation potential of rice to severe terminal drought, effectively enhancing the seed set and grain filling (Bahuguna et al 2018) The study attributed the reductions in drought-induced losses in primed rice plants to the higher activity of cell wall invertase and sucrose synthase – associated with sink strength Together, these studies evidenced that cell wall invertases play wide-ranging roles in encouraging different aspects of rice reproductive development by assuring a steady sink strength under drought In drought-stressed rice plants, some other cell wallrelated proteins have been identified, which are associated with anther wall degradation, such as cysteine protease, adenosine kinase, pectinesterase inhibitor, β-expansin etc (Liu and Bennett 2011) Since pollen grains develop inside the anther wall, and because anther dehiscence and pollen release depend largely on the degradation of anther wall (Koltunow et  al 1990; Scott et  al 1991), the identified proteins may have a crucial role in pollen development and reproductive success of rice under drought Therefore, to comprehensively advance our mechanistic understanding of the reproductive success of rice under drought, we must functionally characterize the different above-reviewed putative cell wall-related genes This will lead to the identification of drought-responsive molecular mechanisms and pathways operating spatiotemporally across different phases of the reproductive stage of rice under drought (Wang et al 2010) In turn, these efforts can create novel avenues towards the rapid development of highyielding drought-tolerant rice varieties Importantly, almost all the studies have analyzed the role of male gametophyte in the reproductive growth of rice under drought, leaving the role of female gametophyte unexplored Plant Cell Reports (2021) 40:437–459 Co‑localized drought‑responsive genes and quantitative trait loci (QTLs) associated with cell wall dynamics in rice Through the analysis of gene expression and genetic map data, the differentially expressed putative genes, underlying the regulation of complex quantitative traits, can be mapped against the QTLs for corresponding traits Co-localizing the candidate genes to their corresponding QTLs can help in the identification of putative genomic regions potentially associated with different agronomically important quantitative traits In addition to the candidate genes reviewed in the earlier sections of this review, several other cell wall-related droughtresponsive genes have also been identified that co-localize with QTLs governing morpho-physiological traits directly or indirectly associated with drought tolerance of rice These genes act as major candidate genes for the function of corresponding QTLs A large-effect QTL, DTY12.1, governing rice grain yield during the reproductive stage under drought has been identified on chromosome 12 (Bernier et al 2007) An in-silico network analysis of the region containing this QTL has led to the identification of six candidate genes, including cellulose synthase 10 (CesA10) gene, which is involved in primary cell wall synthesis and contributes to the root hair elongation and improved water uptake in rice under drought (Narciso et al 2010) Through molecular and phenotypic analyses, the study also found that the rice genotypes possessing DTY12.1 showed the presence of CesA10, and their roots showed increased cellulose-content, biomass, and length under drought Collectively, these results suggest that CesA10 has a role in the DTY12.1-mediated improvement in the grain yield under drought in rice Using saturation mapping and differential display, Nguyen et al (2004) identified several putative candidate genes linked to QTLs for drought tolerance-related traits in rice, such as osmotic adjustment, root thickness, root penetration, and total root dry weight The authors report that a cell wall biogenesis-related gene I12A1 (encoding a UDPglucose 4-epimerase homolog) is linked, as a major candidate gene, to prt7.1/brt7.1 QTL region governing basal thickness and penetration of roots, implying that I12A1 might play a pivotal role in drought tolerance of rice by contributing to the cell wall thickening and facilitating the deeper penetration of roots into the substratum for efficient water uptake under water-limited conditions In another study, an acireductone dioxygenaseencoding gene OsARD4 has been demonstrated to improve root architecture by facilitating the development of secondary roots in rice (Ramanathan et al 2018) The study showed that overexpression of the OsARD4 allele from a deep-rooted drought-tolerant landrace (Nootripathu) in a shallow-rooted drought-sensitive rice genotype (ASD16) resulted in early initiation, profuse branching, increased depth, and high biomass of roots—traits closely associated with efficient water uptake 451 under drought In the same study, OsARD4 was found to be linked to the QTLs governing various root growth-related traits such as length, thickness, and penetration ability, implicating that OsARD4 might play a role as a major candidate gene for the function of these root growth-related QTLs Although the authors have not directly ascribed the OsARD4-mediated altered root plasticity to the cell wall modification, a separate transcriptomic study has revealed significant upregulation of some cell wall-related genes in the roots of Nootripathu under drought conditions (Muthurajan et al 2018), indicating that OsARD4 might possibly affect the expression of these cell wall-related genes, and that OsARD4 might possibly be associated with promoting cell wall modification for the accelerated root growth in Nootripathu under drought From these results, it can be suggested that OsARD4 alters the root plasticity in transgenic plants, possibly by remodeling the cell wall structure Examination of QTLs for various seedling morphological traits under different water supply conditions has revealed that several cell wall-related candidate genes, involved in cell wall loosening (extensin and EGase) and cell expansion (OsEXP1, OsEXP2, and OsEXP4), mapped to QTLs governing seedling traits such as adventitious root length, shoot height, shoot biomass, root-shoot dry weight, etc (Zheng et al 2008) These results indicate that these cell wall-related genes might play a vital role in stimulating the growth and elongation of rice seedlings under water-deficient conditions A similar study for QTL and candidate gene mapping reported that two genes for cell-wall loosening, OsEXP2, and EGase, respectively, co-localize with the QTLs governing seminal root length and lateral root length under water-limited conditions (Zheng et al 2003) The study also showed that these cell wall-related genes were upregulated in the seminal root tips under drought Together, these results imply that OsEXP2 and EGase are important candidates for promoting the seminal and lateral root elongation in rice under drought conditions In a genome-wide association study, new QTLs for water deficit tolerance and their linked drought-responsive genes have been identified at the vegetative stage of rice (Hoang et al 2019) Among these QTL-linked genes, a non-specific LTP coding gene, OsLTPG20, was found to be located within q6 QTL (associated with relative water content) The study proposes that OsLTPG20 contributes to the modification of the external cell walls for better adaptation to water deficit The application of different types of exogenous ameliorants is very beneficial for the growth and development of rice plants under environmental stresses (Reviewed by Ganie et al (2019)) Apart from all the studies evaluated so far in this review, a different study has reported that the application of silicon to rice plants enhances the levels of carbohydrates in the leaf cell walls, which considerably minimizes the electrolyte leakage from the cells under water deficit (Agarie et al 1998) The reduction of electrolyte leakage in leaves indicates that silicon can help in maintaining the photosynthetic capacity 13 452 under drought Besides silicon, we need to look for more exogenous ameliorants that can alter the structure and function of the cell wall for enhanced drought tolerance of rice Resurrection plants: potential genetic resources for cell wall modulation‑mediated drought tolerance in rice Dehydration stress causes metabolic disruption and severely limits growth and reproduction in plants However, a unique group of vascular angiosperm plants, called resurrection plants, possesses a remarkably high ability to tolerate extreme levels of dehydration during prolonged periods of severe drought and regain full physiological and metabolic competence following rehydration (Gechev et al 2014) The drought tolerance of some of these plants is so fascinating that even a detached leaf or leaf segment can survive the severe dehydration to regenerate a new plant (Xiao et al 2015) Extreme dehydration leads to mechanical stress in plant cells and tissues by causing tearing of plasmalemma, cell shrinkage, and a considerable reduction in cell volume (Farrant 2000) One of the strategies that resurrection plants employ to cope with these dehydration effects is the mechanical stabilization of cells by modifying their cell wall architecture (Dinakar et al 2012) Several types of modifications for stabilizing the cell wall structure under dehydration stress have been reported to occur in resurrection plants (Reviewed in Dinakar et al (2012) and Tenhaken (2015)) Keeping in view the extraordinary cell wall modifying mechanisms of these land plants for surviving severe dehydration, it would be highly rational to identify the associated genomic resources regulating such mechanisms for the purpose of engineering drought tolerance in cereal crops Some studies have characterized the cell wall-related resurrection (CWR) genes for drought tolerance (Cho et al 2006; Wang et al 2009; Choi et al 2011; Dai et al 2012; Giarola et al 2016; Mbinda et al 2019), while the other studies reporting on the identification of drought-responsive CWR genes are based on transcriptomics (Jones and McQueen-Mason 2004; Georgieva et al 2010; Jiang et al 2012; Gu et al 2019) Furthermore, CWR genes have been used to engineer drought tolerance in different plant species, such as Capsicum annuum CaXTH3 and Rosa hybrida RhEXPA4 genes in Arabidopsis (Cho et al 2006; Dai et al 2012), CaXTH3 in tomato (Choi et al 2011), and Xerophyta viscosa XvSap1 in sweet potato (Mbinda et al 2019) However, we believe that avenues are completely open concerning the engineering of rice drought tolerance using these genes We did a BLAST (blastn) search at NCBI using these CWR genes as queries with the aim to find their potential homologues (the top most matching hit) in rice, and we observed a significant sequence similarity in each 13 Plant Cell Reports (2021) 40:437–459 case: Expansin-A4-like (XM_015785368.2) showing 71% sequence similarity and 50% query coverage with RhEXPA4, cold acclimation WCOR413-like (AF283006.1) showing 65% similarity and 64% coverage with Xvsap1, and OsXET22 (XM_015785621.2) showing 71% similarity and 52% coverage with CaXTH3 Although the function of these rice genes is similar to that of their CWR counterparts, the latter are superior in accomplishing these functions which may be attributed to their sequence variations Nonetheless, the significant sequence similarity of these genes indicates that the general mechanisms of maintaining the mechanical strength and flexibility of the cell wall under drought are potentially conserved in resurrection plants and rice Besides the major mechanism of cell wall folding, the resurrection plants are superior to rice and other plants in attaining the mechanical stabilization of their cell walls, likely due to the large amount of pectic substances and calcium, and the signature alterations in the content and structure of specific polysaccharides (Dinakar et al 2012) Therefore, based on these points, the CWR genes that would be isolated in the future and those reported in the above-mentioned studies can be potentially used for developing highly drought-tolerant elite rice cultivars in future breeding endeavors Besides resurrection plants, wild species of rice also represent absolutely essential genetic resources for the rice drought tolerance improvement (Pham et al 2006; Agustin et al 2011; Singh et al 2015; Neelam et al 2018), because they are adapted to wide-ranging biogeographical stressprone areas and they possess a priceless pool of potential genomic resources for stress tolerance improvement of rice (Ganie et al 2020) However, the potential of these genetic resources for the improvement of cell wall architecture in rice under drought has also remained virtually untapped Most of the data integrated into this review come from the transcriptomic studies, but the studies on ultrastructural or biochemical changes in rice cell wall under drought are highly deficient Although many papers on other plant species report on the changes in structure, composition, and properties of cell wall under abiotic stresses, only some of them provide evidence of involvement of cell wall metabolism genes and enzymes in these abiotic stress-induced changes in the cell wall We briefly discuss the results about the changes in cell wall structure from these studies and put this additional information into the context of rice to indicate possible reasons that transcriptional changes in cell wall modifying genes analyzed in this review could potentially lead to actual changes in cell wall structure or mechanical properties Some of these studies have investigated the changes in cell wall structure and composition under different abiotic stresses and showed the involvement of cell wall modifying genes or enzymes in these changes For example, salt Plant Cell Reports (2021) 40:437–459 stress induces changes in the chemical composition of the cell wall of specific root cells, hinders the function of pectin, enhances deposition of lignin and suberin, and alters cellulose microfibril orientation by affecting cell wall modifying enzymes such as EGases, EXPs, XTHs, and PMEs (Byrt et al 2018) Adaptation of maize roots to low water potentials is due to the more extensible apical root cell walls, which is accomplished in part by increased activity of cell wall metabolism enzymes, including EXP and XET (Wu and Cosgrove 2000) Besides, investigation of cell wall metabolism under cold stress in Pisum sativum genotypes with contrasted freezing tolerance has revealed a differential abundance of esterified pectic polymers and modification of pectin side-chain substitution, which was associated with alterations in the activity of pectin-modifying enzymes including PME and PG during cold acclimation (Baldwin et al 2014) Furthermore, the functional integrity of the cell wall is impaired by cellulose biosynthesis inhibition (CBI), and this specific stress has been shown to cause an increase in arabinose and uronic acid content as well as the lignin deposition in seedling cell walls (Hamann et al 2009) This change in the cell wall composition was found to correlate with the increased expression of genes for lignin and cell-wall polysaccharide biosynthesis, such as CCR7-like, OPCL1, and UXE4, whereas the expansin genes (ATEXP3 and 11) and genes encoding arabinogalactan proteins (AGP4 and 14) were downregulated Other studies have functionally characterized different types of abiotic stress-related genes for cell wall metabolism and their interactions with their target cell wall modifying genes or the associated changes in the expression of these target genes For example, ectopic expression of a soybean stress-inducible RD22-like gene (GmRD22) alleviates salinity and drought stress in transgenic rice and Arabidopsis due to the increased lignin production in their cell walls (Wang et al 2012) GmRD22 was demonstrated to interact with cell wall peroxidase GmPer1 to strengthen cell wall integrity under abiotic stress conditions Functional analysis of XTH30 reveals a crucial role of this gene in affecting salt tolerance of Arabidopsis by modulating xyloglucan structure, the abundance of xyloglucan-derived oligosaccharide, cellulose-content, and depolymerization of cortical microtubules in response to salt stress (Yan et al 2019) Cell wall integrity maintenance and salt tolerance in Arabidopsis are contributed by histone acetyltransferase GENERAL CONTROL NON-REPRESSED PROTEIN (GCN5), which acetylates three cellulose synthesis genes including CHITINASELIKE (CTL1), POLYGALACTURONASE INVOLVED IN EXPANSION-3 (PGX3) and MYB DOMAIN PROTEIN-54 (MYB54), leading to the alterations in primary wall cellulose synthesis and deposition (Zheng et al 2019) High salinity also causes softening of root cell walls and FERONIA (FER), a plasma-membrane localized receptor kinase, 453 reverses this effect In the salt-stressed fer mutants, the root cells explode due to the disruption of pectin cross-linking (Feng et al 2018), indicating that enzymes facilitating pectin cross-linking may promote the cell wall integrity under salt stress Mutation in arabinose biosynthesis gene MUR4 has been demonstrated to cause reduced root elongation phenotype and cell bursting under salt stress (Zhao et al 2019) These effects on the salt-stressed mur4 mutant plants were shown to be due to the disruption in the cell wall structure in primary root cells owing to the reduced arabinose-content and alterations in AGPs in cell walls Besides, the overexpression of an MYB transcription factor gene from Betula platyphylla (BplMYB46) leads to improved salt and osmotic stress tolerance in transgenic plants (Guo et al 2017) The transgenic plants exhibited increased lignin deposition, higher cellulose-content, and lower hemicellulose-content in their secondary cell wall, which was shown to be due to the altered expression of lignin, cellulose and hemicellulose biosynthesis genes such as phenylalanine ammonia lyase (PAL), caffeoyl-CoA O-methyltransferase (CCoAOMT), 4-coumarate-coa ligase (4CL), Laccase (LAC), cinnamoylCoA reductase (CCR​), cellulose synthase (CESA), fragile fibre (FRA) and irregular xylem (IRX) Similarly, salt and osmotic stresses induce higher expression levels of lignin biosynthetic genes and promote lignin accumulation in the cell walls of BpNAC012 overexpression lines for enhanced tolerance to these stress conditions (Hu et al 2019) Taken together, these results from other plant species about the involvement of different genes and proteins in cell wall metabolism support the notion that changes in the abundance of similar cell wall-related transcripts and proteins of rice analyzed through transcriptomic and proteomic studies can potentially lead to the modification of cell wall structure, composition, and properties Conclusions Like other plants, cell wall plasticity is a common but very important response to drought in rice The flexibility of the cell wall in rice is due to the remodeling in the structure of various cell wall constituents Various genomic resources have been identified underlying the regulation of droughtinduced changes in cell wall architecture in rice at its vegetative and reproductive stages With most of these reports coming from the transcriptomics studies, nonetheless, progress in the analysis of these genomic resources is considerably poor Therefore, to advance our understanding of the vegetative and reproductive success of rice under drought, it is the need of the hour to functionally characterize these genomic resources by employing the state-of-the-art technologies in genomics as well as in quantitative and molecular genetics This will lead to the elucidation of pragmatically 13 454 novel molecular mechanisms and pathways involved in the regulation of drought tolerance at different developmental stages of rice In turn, these efforts would pave the way for devising a realistic genetic engineering approach for developing high-yielding drought-tolerant rice plants Besides identifying and analyzing various genomic resources, sincere efforts should be made to analyze the changes in the rice cell wall structure itself under drought, comparatively an unexplored subject Also, with most of the studies on the reproductive development of rice having analyzed the role of cell wall plasticization-mediated growth of male gametophyte in the reproductive success of rice under drought, attention must also be paid towards analyzing the role of cell wall plasticity-mediated growth of female gametophyte in this process Importantly, we should capitalize on the different CWR genes for engineering the drought tolerance in rice Furthermore, the effect of different types of exogenous ameliorants should also be tested on the structural and functional characteristics of rice cell wall under drought conditions Author contribution statement Conceived and designed the article: SAG Wrote the draft manuscript: SAG Reviewed and edited the manuscript: GJA Both authors have read and approved the manuscript Compliance with ethical standards  Conflict of interest  The authors declared that they have no competing interests with regard to the work reported in 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