Engineering abiotic stress response in plants for biomass production

16 Pages·2017·0.8 MB·English

JBC Papers in Press. Published on January 16, 2018 as Manuscript TM117.000232
The latest version is at http://www.jbc.org/cgi/doi/10.1074/jbc.TM117.000232
Plant biomass under abiotic stress

Engineering abiotic stress response in plants for biomass production
Rohit Joshi1, Sneh L. Singla-Pareek2 and Ashwani Pareek1,3

1 Stress Physiology and Molecular Biology Laboratory, School of Life Sciences,
Jawaharlal Nehru University, New Delhi 110067, India
2 Plant Stress Biology, International Centre for Genetic Engineering and Biotechnology,
Aruna Asaf Ali Marg, New Delhi 110067, India
3 The UWA Institute of Agriculture, School of Agriculture and Environment, The University of Western
Australia, Perth, WA, Australia

Running title: Plant biomass under abiotic stress

To whom correspondence should be addressed: Ashwani Pareek, Stress Physiology and Molecular
Biology Laboratory, School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India,
Telephone: [phone]; E-mail: [email protected]

Abbreviations: ABA, Abscisic Acid; ACC, 1-Aminoyclopropane-1-Carboxylic Acid; ACDS, 1- D
o
Aminocyclopropane-1-Carboxylate Deaminase; BR, Brassinosteroid; BES1, BRI1-EMS-Suppressor-1; w
n
BIN2, Brassinosteroid Insensitive-2; BRI1, Brassinosteroid Receptor Kinase 1; CesA, Cellulose Synthase; loa
d
e
CCR, C-C motif Chemokine Receptors; CK, Cytokinin; CKX, Cytokinin Oxidase; ERF11, Ethylene- d
Responsive Transcription Factor-11; EXPA4, Expansin-A4; EXPB2, Putative Expansin-B2; GA, from
Gibberellins; GSK3, Glycogen Synthase Kinase-3; HDA, Homolog of dnaA; HDC1, Histone Deacetylase http
Complex-1; IAA, Indole Acetic Acid; IPT, IsoPentenyl Transferase; NAC, NAM ATAF1,2 and CUC2; ://w
NCED, 9-Cis-Epoxycarotenoid Dioxygenase; PGPB, Plant Growth Promoting Bacteria; PIKK, w
w
Phosphatidyl Inositol-3-Kinase-related Kinase; pSARK, Senescence Associated Receptor Protein Kinase .jb
c
Promoter; ROS, Reactive Oxygen Species; RXT3, Regulator of Transcription-3; SAM, Shoot Apical .org
Meristem; SPL8, Squamosa Promoter-binding-Like protein-8; Susy, Sucrose Synthase; TORC1/2, Target b/
y
g
Of Rapamycin Complex-1; XTH3, Xyloglucan endoTransglucosylase/Hydrolase-3; YUCCA, Flavin- u
e
s
containing Monooxygenase t o
n
A
p
Keywords: Abiotic stress, biomass, secondary cell wall, phytohormone, plant-microbe interaction ril 8
, 2
0
1
9
ABSTRACT plant-microbe interactions, (ii) cell wall
biosynthesis, and (iii) phytohormone levels. In
One of the major challenges in today’s agriculture addition, and at the same time, employing
is to achieve enhanced plant growth and biomass functional genomics and genetics-based
even under adverse environmental conditions. approaches, a very large number of genes have been
Recent advancements in genetics and molecular identified which play a key role in abiotic stress
biology have enabled identification of a complex tolerance. Our review is an attempt to unveil the
signaling network contributing towards plant crosstalk between the transcriptional circuitries for
growth and development on the one hand and biomass production and abiotic stress response that
abiotic stress response on the other. As an outcome has just started emerging. This knowledge may
of these studies, three major approaches have been serve as a valuable resource to eventually custom
identified having potential to improve biomass design the crop plants for higher biomass
production in plants under abiotic stress conditions. production in a more sustainable manner, in
These approaches deal with having changes in (i) marginal lands under variable climatic conditions.

1
Copyright 2018 by The American Society for Biochemistry and Molecular Biology, Inc.
Plant biomass under abiotic stress

Introduction paper-making as well as bioenergy resources in
Despite considerable success in crop the form of biofuels. As of today, there is a
improvement programs, farmers still lose almost tremendous increase in the demand for plant
20-70% of their potential crop yield because of biomass production due to the expanding human
biotic and abiotic stresses (1). Abiotic stresses are population, inadequate food availability and need
one of the key challenges for plant growth and for bioenergy (12). However, with the ongoing
agricultural productivity in arable lands, with debate on ‘food vs fuel’, we need to reassess the
estimated annual loss of billions of dollars (2, 3). options and the resources available to us. Even if
This challenge is expected to grow enormously we plan to use biofuels to satisfy the 20% of the
with the proposed expansion of agricultural growing demand for oil products, there will be
activities in less fertile and marginal areas, which nothing left to eat. Keeping this fact in mind, it is
is now becoming crucial in satisfying the growing imperative to design our future food crops which
food demands (4). Since about 86% of the will have the potential to give high yield and
freshwater is utilized for the production of biomass even under marginal lands.
agricultural biomass, an additional pressure is Biomass accumulation in plants occurs
likely to come on the fresh water resources with either by an increase in cell number or by cell
the ongoing shifts from the era of ‘fossil energy’ expansion (13, 14). Dissecting out the regulatory
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to the era of ‘energy from biomass’ (5). To keep network involved in cell wall biosynthesis, w
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pace with this alarming situation, novel provides an attractive strategy to improve plant lo
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approaches are vital to enhance plant biomass architecture and biomass (15,16). In recent years, ed
production under adverse environmental considerable attention has also been given to fro
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conditions (6). plant cell wall polymers, which form a major h
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The acclimation of plants to abiotic stress component of plant biomass. The composition ://w
is a complex and coordinated response involving and amount of these polymers in cell wall change w
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hundreds of genes and their interactions with with plant development and in response to stress .jb
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various environmental factors throughout the conditions (17). Further, there is a need to .o
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developmental period of the plant (7, 8, 9). delineate the genes responsible for the b/
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Accordingly, a thorough understanding of the biosynthesis of different cell wall components, g
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molecular responses in plants is essential for along with the assembly and the regulation of cell st o
targeting any improvement in plant biomass or wall dynamics and heterogeneity (17). In addition n A
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either simultaneously or sequentially, under field possibility for improving abiotic stress tolerance 1
9
conditions is indeed a tedious task, but it is the as well as biomass of plants. The third crucial
need of our time (10). However, to minimize the area to be explored for plant biomass
“yield gap” caused by these abiotic stresses, it is enhancement and sustainable agriculture is
vital to understand the gene regulatory networks ‘plant-microbe interaction’. Plant roots and
operating in plants. We hope that the recent microorganisms interact and compete for
advances in molecular biology including tissue or nutrients, making a complex system within the
developmental stage-specific gene expression, rhizosphere (18). However, a complete
stringently regulated and induced gene understanding is needed about the effect of these
expression, site-specific integration of the microbes in improving abiotic stress tolerance
transgene, and gene pyramiding will assist us in and in inducing higher biomass production in
enhancing the photosynthetic efficiency in plants plants (19).
contributing eventually to produce higher One of the goals of our review is to
biomass when grown under marginal lands (11). understand the crucial strategies being developed
The development of human civilization to engineer abiotic stress response and to enhance
is inextricably linked to the plant biomass, where biomass production in plants. Here, the focus is
the wood and the fiber is being used for numerous on the above three major strategies which can be
purposes, including energy production, textiles, utilized to mitigate abiotic stress response,
2
Plant biomass under abiotic stress

besides enhancing biomass production. In this Hormones such as auxins, cytokinins and
review, we present several examples where plant- gibberellins along with other organic compounds
microbe partnerships have been utilized to cope that stimulate cell growth and division under
with the abiotic stress response leading to higher various environmental stresses have also been
biomass production. Further, we discuss recent implicated in such complex interactions (27).
advances in molecular studies that reveal key Schematic diagram depicting the complex
transcriptional switches regulating secondary interaction of PGPB in increasing plant growth
wall biosynthesis under abiotic stress. We also and biomass under stress is shown in Figure 1.
highlight the key facets of the plant growth Various PGPBs possess not only the ability to
regulators having a direct role in the regulation of induce ROS-scavenging enzymes, but also to
plant growth under various abiotic stresses. The increase the photosynthetic efficiency, of plants,
knowledge of these master switches will under abiotic stress, thus leading to enhanced
simultaneously improve our understanding to plant growth (28). Seed priming with these PGPB
develop new strategies to genetically modify the strains significantly improves biomass and
composition and quantity of lignocellulosic nutrient uptake under stress conditions (29).
biomass besides increasing abiotic stress Recently, the multifaceted action of
tolerance. microorganisms has been shown by Khan et al.
(30), where enhanced expression of antioxidant
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(A) Exploiting plant-microbe interactions enzyme machinery through Bacillus pumilus w
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Several studies have demonstrated that inoculation led to improved growth under high lo
a
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plant-microbe interactions influence abiotic salt and boron stress in rice. Furthermore, PGPBs ed
stress tolerance along with growth and biomass. help plants through phytoremediation of fro
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Plants form highly complex and diverse excessive salts, leading to improved biomass h
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associations with co-evolved microbial production under salt stress (31). Bacteria, such ://w
communities (20). Microbial communities show as Pseudomonas spp., Burkholderia caryophylli, w
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plant specificity in terms of their morphology and Achromobacter piechaudii, were shown to reduce .jb
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secondary metabolism (21). Diverse mechanisms endogenous ethylene levels in plants by .o
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have been proposed for varied associations of producing 1-aminocyclopropane-1-carboxylic b/
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plant growth promoting bacteria (PGPB) and acid (ACC)-deaminase, thus resulting in g
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fungal endophytes, after their colonization in the increased root growth, and improved tolerance of st o
rhizosphere/endosphere of plants (22). The plant- salt and water stress (31). In addition, synthesis n A
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mseiqcureosbter aitniotenr,a ncutitorinesn ts icgyncilfiincga,n tpllya natf fgercotw ctahr baondn odfe aImndinoales eA (cAeCtiCc DA)c aidc t(iIvAityA i)n o trh ee nrhhiaznocsipnhge AreC bCy ril 8, 2
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productivity (23, 24) besides ameliorating plant Trichoderma atroviride or Pseudomonas putida 1
9
responses against abiotic stresses (22). Many in tomato results in improved growth and stress
studies have shown that diverse bacterial species, tolerance (32). Similarly, knocking down the
belonging to different genera, contribute towards expression of ACCD gene from T. asperellum
tolerance against various abiotic stresses to the showed reduced root elongation in canola
host plants resulting in enhanced biomass (25). seedlings, suggesting its role in root growth
There is now good evidence from recent promotion (33). Burkholderia phytofirmans
agricultural practices that the use of Plant Growth strain PsJN improves leaf area, chlorophyll
Promoting Bacteria (PFPB) are a strong, viable content, photosynthetic rate and water-use
and vital option to overcome productivity efficiency, ultimately resulting in the enhanced
constraints besides mitigating environmental shoot and root biomass under various abiotic
stresses in crops, e.g., soybean, barley, maize and stress in a wide spectrum of host plants including
rice (26). On the one hand, the microbes induce potato, tomato and grapevine (34).
local or systemic inducible response mechanisms Considerable progress has been made in
in plants to overcome abiotic stress, while, on the unraveling the morphological, physiological and
other hand, they contribute towards sustaining the molecular mechanisms of growth promoting
biomass and growth through - uptake, bacteria mediated abiotic stress tolerance in
mobilization and synthesis of nutrients. plants (35). However, delineating the signaling
3
Plant biomass under abiotic stress

molecules released by PGPB that enhance plant functioning of the cell. For example, plants show
growth and defense responses still remains a higher production of lignin biosynthesis enzymes
challenge. Similarly, extensive research on during abiotic stresses (37). Similarly, severe
enhancing the effectiveness and consistency of dwarfing and altered wood anatomy were
microbial inoculants in multiple-stress observed by silencing 4-coumarate-coenzyme A
amelioration under field conditions will help us ligase, which reduces the lignin content in
in the screening of suitable bio-inoculants to tracheal elements (38). At present, there is fair
improve crop productivity under different interest in unraveling the molecular processes
environmental vagaries (36). Certainly, novel regulating secondary wall development in plants
bacterial strains must be tested in the future to get as it is the most abundant plant biomass in the
better insight into the plant-microbe interaction in form of fiber and timber (39).
order to achieve this target. However, Immense progress has been made for the
encompassing different omics approaches to identification and functional validation of cell
study microbe mediated stress mitigation wall polysaccharide biosynthetic genes
strategies will further strengthen our knowledge (including those for cellulose, glucomannan,
on the mechanisms of plant-microbe interactions xyloglucan, xylan, and pectin), as well as sugar
with the naturally associated or artificially nucleotide donors of these pathways (17). In
inoculated microorganisms. Primary targets for plants, cellulose microfibrils, composed of β-1,4-
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optimizing beneficial plant-microbe interactions glucan chains mainly contribute towards the w
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include quorum sensing, bacterial motility, above-ground biomass and their biosynthesis and lo
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biofilm formation and their signaling pathways. accumulation play a vital role in providing ed
Current evidence supports the plant-microbe defense against climatic vagaries (40). Cellulose fro
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interaction in mitigating abiotic stress response synthase (CesA) gene superfamily regulates the h
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during varied edaphic and climatic conditions. At synthesis of cellulose in plants (40). ://w
present, a range of bacterial formulations are Brassinosteroid signaling activates BES1 w
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already available commercially for their use as transcription factor, which binds to the E-box .jb
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‘bioprotection agents’ or ‘biofertilizers’ to (CANNTG) in the promoter of CesA causing its .o
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improve biomass and yield under biotic stresses. upregulation and thus resulting in enhanced b/
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Utilizing these microorganisms will further cellulose accumulation in Arabidopsis (41). g
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enhance tolerance against various abiotic Similarly, CESA1 kinase activity was shown to be st o
stresses, thus establishing novel and promising enhanced by the degradation of its inhibitor n A
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t echniques for sustainable agriculture. B(4R2A). SISnI NadOdSitTioEnR, OinItDro gIrNeSssEioNnS IoTf IVBER2 re(cBeIpNto2r) ril 8, 2
0
(B) Regulation of cell wall biosynthesis containing chromosome segment (7DL) from 1
9
Around 430 million years ago, vascular Agropyron elongatum results in enhanced
plants appeared on land and co-evolved with the drought tolerance in wheat (43). However,
ability to develop secondary cell wall. Plant cell increase in UDP-Glc (a substrate for synthesis of
wall functions as an ‘exoskeleton’ by providing various sugars, necessary for different wall
mechanical and structural support to the entire polymers) levels by overexpressing sucrose
cell as well as acting as a physical barrier against synthase (SuSy) and UDP-glucose
abiotic and biotic stresses (17, 37). The principle pyrophosphorylase (UGPase) encoding genes
components of a secondary cell wall are leads to enhanced drought tolerance and cellulose
cellulose, hemicelluloses and lignin; accumulation (44). Similarly, heavy metal stress
interestingly, they are quite unique to each cell in rice and wheat causes enhanced lignin
type and vary in their amount and composition accumulation in cell wall, which improves
along with development and in response to defense response against biotic and abiotic
various biotic and abiotic stresses (17, 37). Thus, stresses (45).
we can conclude that plants have inherently Transgenic Arabidopsis plants
evolved intricate mechanisms to regulate overexpressing CaXTH3, encoding a xyloglucan
biosynthetic pathways for cell wall components biosynthesis gene (xyloglucan
and have assembled them for the proper endotransglucosylase/hydrolases), have
4
Plant biomass under abiotic stress

abnormal leaf morphology and severely wrinkled Of the various factors regulating plant
leaf shape and enhanced tolerance against water biomass production under abiotic stresses,
stress (46). β-expansin encoding gene EXPB2 manipulation of plant hormone content is the
showed higher expression under water stress and most efficient approach (53). Of these hormones,
seemed to be involved in improvement of root auxins, cytokinins (CKs), gibberellins (GAs),
system architecture under water deficit in brassinosteroids (BRs) and abscisic acid are
soybean (47). Similarly, silencing of NAC2 or its markedly involved in the regulation of plant
downstream gene EXPA4 has been shown to growth and biomass production during stress
result in reduced drought tolerance during the conditions (53). Figure 3 depicts the crosstalk
petal development in rose (48). In contrast, between various phytohormones leading to
overexpression of RhEXPA4 conferred improved enhanced stress tolerance resulting in higher
phenotype with shorter stems, curly leaves, biomass production in plants. Dissecting the
compact inflorescences and enhanced drought molecular mechanism of these hormone
tolerance in Arabidopsis (48). However, higher biosynthesis and regulation provide an insight
transcript abundance of cinnamoyl-CoA into the complexity of various processes such as
reductase (CCR) in maize inhibited cell wall time, rate and extent of cell division and cell
extensibility and root growth under water expansion to manipulate the regulation of
deficiency (49). Similarly, expansin acts as a key meristematic division and plant growth under
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component in heat stress tolerance as its higher stress conditions (54). While cytokinins (CKs) w
n
expression in Agrostis leads to increased cell wall have an important role in delaying natural lo
a
d
elasticity, which maintains cellular functions senescence in many plants (55), the concentration ed
(50). Arabidopsis MYB41 and rice R2R3-type of the bioactive CKs decreases during exposure fro
m
MYB transcription factor MPS (MULTIPASS) to water and salt stresses (56). h
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are induced under salinity, which then enhances Plants exhibiting negative regulation of ://w
expression of cell wall-biosynthesis genes, during cytokinin activity, such as plants overexpressing w
w
vegetative and reproductive stages, while CKX (CYTOKININ OXIDASE) or mutation in .jb
c
suppressing the transcript of expansin and the cytokinin receptors, show smaller SAM .o
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endoglucanase genes (51). Similarly, (shoot apical meristem) and decreased leaf area b/
y
overexpression of TOR, a Ser/Thr kinase of the (57). Similarly, it is known that knocking down g
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phosphatidylinositol-3-kinase-related kinase CKX2 expression in rice results in the st o
(PIKK) family leads to enhanced cellular biomass maintenance of photosynthetic rate, panicle n A
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0
(52). on transgenic plants with pSARK promoter 1
9
Integrating the knowledge of key regulated isopentenyltransferase (IPT) gene
regulatory genes with their cell-specific expression have reported delayed leaf
promoters and transcriptional regulation of senescence, higher photosynthetic activity and
secondary cell wall biosynthesis through the enhanced biomass and/or yield-related
cascade of activators, repressors and feedback parameters under drought stress in tobacco (59),
regulators is expected to enable the development rice (60), broad bean (61), creeping bent grass
of designer plants with enhanced biomass under (62), peanut (63) and under salt stress in cotton
stress conditions (16,17). Schematic diagram (64).
depicting the transcriptional regulatory network Under heavy metal and salt stress, IAA
modulating secondary cell wall formation in increases shoot as well as root growth in plants
plants is shown as Figure 2. These studies also (27). Transgenic poplars overexpressing an
provide deep insight into the complex abiotic stress responsive YUCCA6 gene, which is
transcriptional machinery to genetically modify involved in tryptophan-dependent IAA
cell wall composition for tolerance against abiotic biosynthesis pathway using stress-inducible
stresses. SWPA2 promoter, exhibit rapid shoot elongation
and reduced main root development with
(C) Manipulation of phytohormone levels enhanced root hair formation (65). Earlier studies
5
Plant biomass under abiotic stress

demonstrated that down-regulation of SPL8 xanthoxin. In addition, T-DNA insertional nced3
(Squamosa Promoter-binding-Like protein-8) mutants displayed impaired drought tolerance
transcription factor significantly increased and limited ABA accumulation under water
branching by promoting axillary bud stress, while tobacco plants constitutively
development and enhanced forage biomass yield, expressing NCED1 enhanced ABA accumulation
besides enhancing salt and drought tolerance in in leaves, which leads to improved drought and
alfalfa (66); these transgenic plants showed salt stress tolerance (75). Similarly, in tomato
reduced GA accumulation, while spl8 mutants constitutive overexpression of NCED1 displayed
showed significantly higher GA transcript enhanced ABA accumulation, reduction in
abundance. Furthermore, GA2-ox6, which is the assimilation rates, leaf chlorosis and higher
prime GA deactivation enzyme, is significantly biomass because of counteracting positive effects
up-regulated by SPL8 (66). These results suggest of ABA on leaf expansion and increased water
that SPL8 regulates GA signaling, and GA2-ox is status (76).
a possible key node of this signaling network Similarly, brassinosteroid (BR) pre-
(67). Under saline conditions, GA application treated seeds demonstrated significantly higher
improved stomatal conductance, water use accumulation of dry mass and antioxidant
efficiency, growth and yield in tomato plants, enzyme activity in alfalfa under salt stress (77)
thus supporting the above hypothesis (68). and ameliorated growth and survival of Robinia
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The Arabidopsis homolog of RXT3 pseudoacacia during water stress (78). In w
n
(REGULATOR of TRANSCRIPTION 3), named addition, BR application causes enhanced lo
a
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HISTONE DEACETYLASE COMPLEX1 seedling growth in sorghum under osmotic stress ed
(HDC1) shows direct interaction with histone (79). Knockout T-DNA insertion mutant of fro
m
deacetylases HDA6 and HDA19 (69). The hda6, Osgsk1 (a rice GSK3/SHAGGY-like protein h
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hda19 and hdc1-1 mutant showed kinase gene, ortholog of AtBIN2/AtSK21, a ://w
hypersensitivity towards NaCl and ABA during negative regulator of BR-signaling), depicted w
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seedling stage (69). However, HDC1 enhanced tolerance towards abiotic stress, while .jb
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overexpression reduces NaCl and ABA OsGSK1 overexpression resulted in stunted .o
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sensitivity and increases biomass (70). growth in Arabidopsis (80). In addition, b/
y
Transgenic tomato plants overexpressing abscisic hormones target various members of protein g
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acid (ABA) responsive complex (ABRC1) form families playing a significant role in growth st o
barley HVA22 gene, maintained growth and yield either individually or in co-regulated manner, n A
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b(7e1si)d. esF utortlheerarmtinogr e,c olAdt,E dRrFo1u1g htw aansd sshalotw sntr etsos tmheetraebboyl ici ndpicaatthiwnga yst he (8s1y)n. ergBisiotitce chancotiloong icoafl ril 8, 2
0
negatively modulate the ABA-mediated manipulation of these key proteins could allow 1
9
regulation of ethylene biosynthesis; further, its not only the adaptation under adverse
overexpression conferred ABA hypersensitivity environmental conditions, but also determine the
during post-germination growth under stress flux in phytohormone biosynthesis for securing,
conditions (72). ABA3/LOS5 encodes a Mo- in the long run, improved food production.
cofactor sulfurase (MCSU) that catalyzes
abscisic aldehyde to ABA conversion and its Future Outlook
constitutive expression in rice leads to With the apparent changes in the global
significantly higher yield during drought stress environment, agricultural production systems are
under field conditions (73). Similarly, liable to change. Thus, there may be a need to
overexpression of MoCo sulfurase gene in produce cost-effective biomass to replace the
soybean resulted in enhanced biomass and yield existing fossil fuel in the near future. At the same
along with improved drought tolerance attributed time, to ensure availability of enough food for 9
to increased ABA accumulation, reduced water billion people is indeed a daunting task. One
loss and induced antioxidant enzymatic possible solution to this challenge could be to
machinery (74). Furthermore, 9-cis-epoxy make use of marginal lands with low input crops
carotenoid dioxygenase (NCED) has been shown capable of providing high-biomass yield.
to catalyze the conversion of neoxanthin to Attempts are already being made to modify the
6
Plant biomass under abiotic stress

plant architecture in such a way that will led to Indo-US Science and Technology Forum
‘transgressive overyielding’ of plant biomass. (IUSSTF) for Indo-US Advanced Bioenergy
Further, there are numerous options to explore Consortium (IUABC). Research in the lab of AP
plant-microbe interactions for enhanced biomass is also supported from funds received from
production in marginal and arable lands. It is International Atomic Energy Agency (Vienna),
noteworthy that the most of these interactions are UGC-RNW and UPE-II (India). Authors
currently unexplored, making it important to gratefully thank Professor Govindjee, University
closely observe the soil, the rhizosphere and the of Illinois at Urbana-Champaign for critical
endophyte populations. Engineered plants and reading of the manuscript.
their beneficial symbionts will pave the way for Conflict of Interest: The authors declare that
future strategies to modify them for higher they have no conflicts of interest.
biomass production to meet the demands of
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RJ acknowledges Dr D S Kothari Postdoctoral Rep. 7, 9287
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