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Plant Gene 25 (2021) 100264
Available online 28 November 2020
2352-4073/Published by Elsevier B.V.
An overview of recent advancement in phytohormones-mediated stress
management and drought tolerance in crop plants
Chhaya
a
, Bindu Yadav
b
, Abhimanyu Jogawat
c
, Prabu Gnanasekaran
d
, Pratibha Kumari
e
,
Nita Lakra
f
, Shambhu Krishan Lal
g
, Jogendra Pawar
b
, Om Prakash Narayan
h
,
*
a
Department of Civil and Environmental Engineering, IIT Patna, India
b
School of Environmental Sciences, Jawaharlal Nehru University, New Delhi, India
c
National Institute of Plant Genome Research, New Delhi, India
d
Department of Plant Pathology, Washington State University, Pullman, WA, USA
e
Leibniz Institute of Plant Biochemistry, Martin Luther University, Halle (Saale), Germany
f
Department of Biotechnology, CCS HAU, Hisar, India
g
ICAR-Indian Institute of Agricultural Biotechnology, Ranchi, Jharkhand, India
h
BME Department, Tufts University, Medford, MA, USA
ARTICLE INFO
Keywords:
Abiotic stress
Biotic stress
Crop improvement
Plant hormones
ABSTRACT
Plants face a continuous threat of abiotic stresses under the changing environment. Because of climate change,
water scarcity has been shown to be a signicant environmental constraint on plant productivity. Droughts in
particular have been shown to affect plant growth and development, lead to alteration in quality and quantity of
crop production, and result in global food insecurity. Phytohormones are known to play critical roles in regu-
lating diverse processes of plant adaption to a drought environment. They regulate cellular functions at mo-
lecular levels via various cell signaling. Among various phytohormones, abscisic acid (ABA) is known for its role
in drought-stress tolerance in plants. Other phytohormones such as auxins, brassinosteroids (BRs), cytokinins
(CK), ethylene (ET), gibberellins (GA), jasmonic acid (JA), and salicylic acid (SA) are also crucial in plant drought
tolerance. Several plant growth-promoting microbes have been reported to enhance the phytohormone levels in
plants to mitigate the negative effect of drought. However, the transgenic approach appears to be a boon to
engineering the genes responsible for regulating phytohormones to develop a drought-tolerant trait. Expression
analyses have revealed that genes encoding transcription factors such as bZIP11, DREB2, MYB14, MYB48,
WRKY2, WRKY56, WRKY108715, and RD22 play a very crucial role in phytohormone mediated drought
response. Furthermore, exogenous applications of phytohormones are shown to enhance endogenous phyto-
hormones. This review highlights the most recent advancements in phytohormone-mediated drought tolerance in
major crop plants.
1. Introduction
The growth and development of plants is a combined effect of
developmental cues as well as extracellular factors. Stress is generally
described as one of the extracellular factors that adversely affect plant
growth and development, including crop quality and yield. In this re-
view, we discuss the inuence of abiotic stressors on plant growth and
development. Among these stressors, drought is one of the most signif-
icant in limiting crop production worldwide. Drought is a prolonged dry
state in the natural climatic cycle, which occurs when the atmospheric
conditions cause a continuous loss of available water in the soil to a
critical level. In tropical countries, drought is one of the severe con-
straints on crop production due to the rainfall decit that leads to an
adverse impact on people’s livelihoods. It has been reported that around
15 million people were affected by a long-term drought that occurred
during 2005–2006 in the greater horn of Africa (WHO 2020). According
to a WHO report, an estimated 55 million people are inuenced by
drought every year globally (WHO 2020). Moreover, water scarcity af-
fects 40% of the global population, and approximately seven-hundred
million human beings are at risk of being displaced by 2030 (WHO
2020). In the last 50 years, around 67% of crop losses recorded in the U.
S. were due to drought-related-stress (Comas et al., 2013). Yield
* Corresponding author.
E-mail address: om.narayan@tufts.edu (O.P. Narayan).
Contents lists available at ScienceDirect
Plant Gene
journal homepage: www.elsevier.com/locate/plantgene
https://doi.org/10.1016/j.plgene.2020.100264
Received 14 September 2020; Received in revised form 22 November 2020; Accepted 23 November 2020
Plant Gene 25 (2021) 100264
2
reductions of 21% and 40% in wheat and maize, respectively, have been
reported between the years 1980–2015 (Daryanto et al., 2016). It is
estimated that >50% of global major crop yield reduction will occur by
2050 (Li et al., 2009).
The major portion of the human diet is delivered by three distinct
types of crops: cereals, legumes and roots/tubers. Rice, wheat, and
maize are three major cereal grains; oat, sorghum, barley, rye, and millet
are other minor cereal grains consumed worldwide, which account for
around 50% of proteins and 56% of food energy consumed on earth
(Cordain, 1999). Legumes ranked second in respect to food production,
contributing upto 27% of the global primary crop production, providing
33% of protein needs, and contributing to around 35% of the world’s
vegetable oil production (Graham and Vance, 2003).
Aquaporins are water protein channels that facilitate efcient water
transport across the cellular membranes and plasma membrane in many
plants that play a signicant role in plant water relations. This water
ow is driven by the water potential (the sum of pressure, gravimetric,
matric potential, osmotic, and air pressure) difference between the soil
and atmosphere (Scharwies and Dinneny, 2019). Major water deciency
occurs due to the disproportionate water uptake from the soil and water
lost through transpiration. These factors can cause turgor loss of the
entire tissue and wilting (Scharwies and Dinneny, 2019). Furthermore,
studies have reported that the stored water volume drops upto 40%
during water stress conditions (Waring and Running, 1978). Drought
stress causes an increase in leaf osmotic pressure, which leads to the
reduction of transpiration, stomatal conductance, turgor pressure, and
water potential in leaves, as well as the reduction of osmotic hydraulic
conductance and sap ow rate in the roots (Mahdieh et al., 2008).
Altogether, drought affects the plant-water relationship, which makes
plants unstable, and thus, affects plant growth and development (Pareek
et al., 2010).
Plants respond to drought-related stress by alterations in several
morphological, biochemical, and physiological processes (Farooq et al.,
2009b; Kapoor et al., 2020). These changes include the altered tran-
scriptome, proteome, and metabolome of plants that result in revised
cellular biosynthesis and degradation activities of proline and several
enzymes. Drought inhibits leaf expansion and lowers the photosynthetic
rate, which ultimately inuences plant growth and biomass accumula-
tion as well as causing oxidative stress (Anjum et al., 2017; Ohashi et al.,
2014; Sharma et al., 2019a; Tardieu et al., 2014). In general, the effect of
drought stress mainly depends upon species, genotype, size, age, as well
as the time and intensity of stress (Le Gall et al., 2015). Overall, drought
stress adversely affects plant height, ber quality, node number, canopy,
leaf area index, stem, leaf dry weight, plant growth development, and
root development (Davis et al., 2014; Wang et al., 2019b). The reduced
plant growth and yield under drought stress are controlled by various
factors that include phytohormones signaling, ROS signaling, plant hy-
draulic status, and osmotic adjustment (Khan et al., 2015; Tardieu et al.,
2014).
Phytohormones are also known to play a crucial role in acclimati-
zation in response to several biotic and abiotic stressors (Ullah et al.,
2017). In response to drought-related stress, many of these phytohor-
mones are synthesized to help regulate processes associated with
drought tolerance mechanisms in plants. Phytohormones such as ABA,
ET, JA, and SA play roles in the drought-related processes, including
osmotic adjustment (Vishwakarma et al., 2017). These phytohormones
act as chemical messengers in response to several abiotic stressors that
lead to the activation of diverse plant physiological processes, including
accumulation of osmolyte, stomatal closure, and root growth stimula-
tion to avoid water loss (Sharma et al., 2019b; Ullah et al., 2018).
This review discussed the role of various phytohormones and recent
advancements in phytohormone-mediated drought tolerance in major
crop plants. The review mainly conferred on engineered genes respon-
sible for the synthesis of phytohormones in response to different stresses
and the exogenous application of phytohormones, mitigating the nega-
tive effect of drought.
2. Effect of drought stress in major cereal crops
Rice, wheat, and maize are three major cereal grains consumed
worldwide, accounting for more than 55% of food energy (Cordain,
1999). In the last few decades, several major drought events have
occurred, making farming extremely challenging in several countries
(Table 1).
Among all cereal crops, rice is a basic food for more than half of the
world’s population and accounts for greater than 40% of the daily
caloric intake (Fairhurst and Dobermann, 2002). In 2018, rice accoun-
ted for around 29% of total cereal utilization, with global production of
more than 782 million tons (Faostat 2018). During the plant reproduc-
tive phase, drought stress has been reported to affect several biological
processes in leaves, including energy metabolism, redox balance, and
proteins level (Wang et al., 2017a, 2017b). Drought stress decreases
starch content in matured grains, induces early plant senescence, in-
hibits seed germination and seedling establishment, reduces spikelet
fertility, as well as affecting distribution and degradation of indole acetic
acid (IAA) and CK molecules (Chen et al., 2018; Liu et al., 2019; Todaka
et al., 2017; Pratap et al., 2019).
Wheat production ranks rst in global grain production and is
consumed as the predominant food by more than 36% of the world
population (Hasanuzzaman et al., 2018). Drought stress decreases the
chlorophyll contents, spike length, plant height, root and shoot dry
biomasses, grain yield, and gas exchange. It also causes hormonal
imbalance, reduces antioxidant enzyme activities, and causes oxidative
stress (Abbas et al., 2018; Raheem et al., 2018). Moreover, it remarkably
slows down the rate of metabolic processes, photosynthesis, nutrient
assimilation, which ultimately decreases plant growth, and yield
(Hasanuzzaman et al., 2018).
Maize ranked second after wheat and third to rice in terms of pro-
duction worldwide. However, it ranked rst in developing countries like
Africa and Latin America, but ranked third, after rice and wheat, in Asia
(Dowswell, 2019). Drought is one of the signicant factors that limits
global maize production. It is estimated that a 39.3% reduction in maize
yield was due to a 40% water reduction (Daryanto et al., 2016).
Droughts are found to affect gynoecium development and kernel set. It
also represses the leaf growth, alters photosynthesis, and causing an
imbalance of reactive oxygen species (Danilevskaya et al., 2019; Zhang
et al., 2018a, 2018b; Zhao et al., 2016)
3. Phytohormones and their role in stress management
Phytohormones inuence various physiological processes such as
growth and development, reproduction, longevity, and death for the
normal functioning of the plant. In other words, phytohormones are
chemical messenger that regulate the cellular activities of plants. Auxin
is the rst phytohormone (Went, 1935) and strigolactones are the most
recently identied phytohormones (Gomez-Roldan et al., 2008). Out of
nine identied phytohormones, ve phytohormones, i.e., auxins, ABA,
Table 1
List of major drought events from 1998–2010 across the globe
(WHO 2020).
Region Year
Southern Asia 1998–2001
Australia 2000–2010
Canada 2001
Central America 2002
Western Africa 2002
Southern Africa 2003
United States 2004–2006
Greater Horn of Africa 2005
Brazil 2004–2010
Western Europe 2005
South-eastern South America 2008
China 2009
Chhaya et al.
Plant Gene 25 (2021) 100264
3
CK, ET, and GA are referred as “classical” phytohormones while the
remaining four (i.e., BRs, JA, SA, and strigolactones) are later added to
the growing phytohormonal family (Su et al., 2017). Different forms of
biotic and abiotic stresses, which directly affect the plant’s growth, are
shown in Figure 1. These phytohormones are reported to have an
extensive role in coping with several adverse conditions are illustrated
in Figure 2. Colonization of root with fungi alters the levels of growth
regulators, antioxidants, and ROS that could be a potential area of
investigation (Narayan et al., 2017; Prasad et al., 2019). Moreover, plant
growth-promoting rhizobacteria could be a signicant organism that
could be involved in improving plant tolerance to drought stress by
enhancing endogenous phytohormone.
3.1. Auxin
Auxin synthesis in plants occurs in all tissues such as cotyledons,
leaves, and roots; however, young leaves are reported to have the
highest biosynthetic capacity (Ljung et al., 2001). IAA is the most
Figure 1. Diagrammatic representation showing a ow chart of different forms of biotic and abiotic stresses. Drought is one of the major abiotic stress caused by
various environmental factors which is responsible for an inadequate amount of water content in the soil available for crop plants.
Figure 2. Schematic representation of a general overview to show hormone-mediated stress management. Different types of stresses viz. biotic, abiotic, including
drought stress, trigger the regulated synthesis of phytohormones to cope with various fatalities, including plant growth as well as yield.
Chhaya et al.
Plant Gene 25 (2021) 100264
4
studied endogenous auxins in plants (Kasahara, 2016). Plants synthesize
IAA from both tryptophan and indolic tryptophan precursors via
tryptophan-dependent and tryptophan-independent pathways, respec-
tively (Woodward and Bartel, 2005). Auxin is one of the major phyto-
hormones that regulate numerous aspects of plant growth and
development; and coordinates plant responses to the environment.
Auxin response is primarily concentration-dependent, and different
tissue reacts precisely to the changing amount of exogenous auxins (Fu
et al., 2019). Several studies have reported that local auxins are required
for various developmental processes comprising embryogenesis, endo-
sperm development, oral initiation and patterning, root development.
It was recently discovered that the local auxin biosynthesis and transport
are responsible for ower fertility and root meristem maintenance
(Brumos et al., 2018). It is reported that auxins also promote the rooting
in the cuttings of g plants (Ficus carica) (Patel and Patel, 2018).
Further, auxin biosynthesis is induced in response to various environ-
mental signals, such as temperature, light, toxic metals, and pathogens
(Zhao, 2018). In Solanum lycopersicum, SlILR1, 5, and 6 genes were found
to have auxin conjugate hydrolysis activity that plays a crucial role in
oral pedicel abscission (Fu et al., 2019). Xanthomonas campestris and
Pseudomonas syringae infection cause upregulation of miR167a that
mediated auxin signaling genes in tomato (Jodder et al., 2017). Low
selenium (1 mg/L) increases the auxin synthesis and enhances tolerance
to low phosphorous stress due to overexpression of NtPT2 in Nicotiana
tabacum (Jia et al., 2018).
Auxins positively modulate the ROS metabolism, root architecture,
metabolic homeostasis, and ABA-responsive genes (DREB2A, DREB2B,
RAB18, RD22, RD29A, and RD29B) to enhance drought stress resistance
phenotype (Shi et al., 2014). Auxins are reported to enhance the
expression of IAA8, which promotes the formation of the lateral roots
under water stress conditions. It also down-regulates the Sl-IAA27 genes
that have diverse effects on growth and root development in white
clover (Zhang et al., 2020, 2020). PIN1, PIN3, PIN3b, PIN4, and PIN9
upregulates the auxin transport in response to drought stress, which
promotes lateral root formation in tobacco seedlings (Wang et al.,
2018a, 2018b). Further, auxin-responsive gene TaSAUR75 upregulates
stress-responsive genes such as as AtRD26 and AtDREB2, which play a
signicant role in plant growth and development during water decit
conditions (Guo et al., 2018). Drought induces DREB2A/B expression
that promotes the expression of IAA5/6/19. Further, IAA5/6/19 pro-
motes drought resistance in Arabidopsis (Arabidopsis thaliana) via
maintaining the level of glucosinolates (GLS), consequently promotes
stomatal closure via ROS production (Salehin et al., 2019). The down-
regulation of SlARF4 improves drought tolerance in tomatoes by pro-
moting growth and density of root, maintaining chlorophyll content,
and by increasing soluble sugar content (Bouzroud et al., 2019). It has
also been reported that exogenous IAA treatment signicantly improves
drought tolerance in white clover via increasing ABA and JA content as
well as by up-regulating the expression of drought stress-responsive
genes (bZIP11, DREB2, MYB14, MYB48, WRKY2, WRKY56,
WRKY108715, and RD22), auxin-responsive genes (GH3.1, GH3.9,
IAA8) and down-regulating expressions of leaf senescence genes
(SAG101 and SAG102) and auxin responding genes (GH3.3, GH3.6,
IAA27) (Zhang et al., 2020, 2020). We conclude that IAA is actively
involved in the drought stress management via activation of other stress-
responsive hormones as well as the production of ROS. The generation of
ROS results in the regulation of several physiological changes that save a
plant from drought stress.
3.2. Abscisic acid
Abscisic acid is 15 carbon atom compound, belong to a group of
metabolites, known as isoprenoids or terpenoids, which are synthesized
in the plastids (Xiong and Zhu, 2003). ABA in higher plants is synthe-
sized from an indirect pathway through the cleavage of a C
40
carotenoid
precursor, followed by a two-step conversion of the intermediate
xanthoxin to ABA via ABA-aldehyde (Xiong and Zhu, 2003). ABA reg-
ulates a diverse range of cellular and molecular processes during plant
development. It plays an essential role in the regulation of xylem ber
differentiation (Campbell et al., 2018). It has also been suggested to play
a predominant role in seed germination, plant growth, and seed matu-
ration (Yan and Chen, 2016). It is reported that the genes involved in
metabolism and signaling of ABA along with GA are crucial for main-
taining the bud activity-dormancy transition in Camellia sinensis (Yue
et al., 2018). ABA regulates gene expression related to cell wall modi-
cation and anthocyanin biosynthesis in the ripening fruits of Vaccinium
myrtillus L. (Karppinen et al., 2018). It is also one of the known stress
hormones that provide resistance against abiotic stressors, including
drought, heat, cold, and salt, inclusive of enhancement of stress toler-
ance in vascular plants and bryophytes (Cho et al., 2018; Islam et al.,
2018). Plants accumulate ABA in stress conditions, which triggers a
response to cope with the unfavorable environment. It is reported that 4
to 7 times higher level of ABA was present in the levels of seaweed
species, Pyropia orbicularis during the oxidative stress state at the time of
desiccation (Guajardo et al., 2016). Mesophyll cells are shown as the
predominant location of ABA biosynthesis in water-stressed leaves
(McAdam and Brodribb, 2018). In addition, ABA induces resistance
against the bamboo mosaic virus through the expression of AGO2 and
AGO3 (Alazem et al., 2017).
ABA is considered as a signal molecule under drought stress. Upon
plant exposure to drought stress, ABA is synthesized in roots and
translocate to leaves to trigger drought adaptation mechanisms in the
plants such as growth reduction and stomata closure (Qi et al., 2018;
Wilkinson and Davies, 2010). During drought stress, ABA activates
several stress-responsive genes to save plants from water scarcity. For
instance, ABA-activated SnRK2s, which phosphorylate the type-A ARR5
and increase its stability, thus magnifying the ABA-mediated stress
response. Simultaneously, the plant growth is restricted by type-A ARR5
that represses CK signaling via a negative feedback loop in Arabidopsis
(Huang et al., 2018). Overexpression of IbARF5 up-regulates the ABA
biosynthetic genes (IbZEP, IbNCED, and IbABA2) which ultimately
confers drought tolerance in transgenic Arabidopsis (Kang et al., 2018).
Moreover, SAPK2 is the key regulator of ABA-dependent development in
numerous plants. It upregulates the expression of several stress-
responsive genes, including OsLEA3, OsOREB1, OsRab16b, OsRab21,
and OsbZIP23 during drought stress (Lou et al., 2017). All these drought-
regulated genes could be a potential target for the plant’s gene engi-
neering to make them more drought-tolerant.
Further, the upregulation of REL1 coordinates the ABA pathway to
regulate drought tolerance in plants (Liang et al., 2018). Similarly,
overexpression of AtABCG25 stimulates the local ABA responses in
guard cells and improves the water use efciency of plants in water-
decit conditions (Kuromori et al., 2016). Exogenous application of S-
ABA was reported to enhance the antioxidant enzyme activity, expres-
sion of ASR1, endogenous ABA level, as well as reduces oxidative
damage and allows the maize seedlings to alleviate the negative effect of
drought (Yao et al., 2019). Studies on the model plant Arabidopsis and
other plants indicate that ABA is a major drought-responsive plant
hormone directly involved in drought stress management. ABA mainly
regulates stomatal closure to avoid water loss, and the genes involved in
the stomatal closure could be a signicant target to manipulate in order
to improve drought resistant plants.
3.3. Cytokinins
Cytokinins are adenine derivatives with isoprenoid as side chains to
the N
6
position of the adenine ring. Zeatin, isopentenyl adenine, and
dihydrozeatin are the chief CK reported in higher plants; however,
zeatin is the most prevalent CK present in higher plants (Kieber and
Schaller, 2018). The main steps in the biosynthetic pathway for CK
include the transfer of isopentenyl group from dimethylallyl diphos-
phate to ATP, ADP, or AMP, which is catalyzed by isopentenyl
Chhaya et al.
Plant Gene 25 (2021) 100264
5
transferase (Kieber and Schaller, 2014). It was identied in 1950 as a
regulator of cell division (Miller et al., 1955). Further, it supports stem
cell homeostasis in shoot apical meristem and allows plants to respond
and adapt to rapid environmental changes (Landrein et al., 2018). Type-
B Arabidopsis response regulates CK response, which further regulates
diverse aspects of growth and development, responds to biotic and
abiotic factors and promotes leaf senescence in Arabidopsis (Raines
et al., 2016; Zubo et al., 2017). It is noted that CK signaling triggers
primary root growth in Arabidopsis (Naulin et al., 2020). Further, CK
signaling pathway in Arabidopsis is necessary for LZR216-promoted
plant growth and root architecture alteration (Wang et al., 2017a,
2017b). Also, CK plays a signicant role in response to drought, tem-
perature, salt, osmotic, and nutrient stress (Cortleven et al., 2019).
Crosstalk between CK and F-box protein, MAX2 signaling pathways in-
duces growth and callus formation in Arabidopsis (Li et al., 2019).
Similarly, CK signaling promotes callus regeneration in Brassica juncea
(Lu et al., 2020). It is also known to enhance the colonization of sym-
biotic arbuscular mycorrhizal fungi in pea (Goh et al., 2019). CK confer
resistance in Nicotiana tabacum against the Chilli veinal mottle virus (Zou
et al., 2020). Also, CK supports plants’ tolerance against osmotic stress
via the activation of proteins that have negative impacts on growth
(Karunadasa et al., 2020). Trans-zeatin, a CK that is derived from the
root of Arabidopsis, protects the plant against photoperiod stress (Frank
et al., 2020). Osmotic stress induces CK synthesis that antagonizes ABA
signaling and ABA-mediated responses, reduce ROS damage and lipid
peroxidation, delayed leaf senescence, and thus improves osmotic stress
ability of plant and plant growth (Gujjar and Supaibulwatana, 2019).
Up and down-regulation of CK was also reported to enhance drought
tolerance. CK elevation during drought stress diminishes the adverse
effects of stress on photosynthesis (Prerostova et al., 2018). CK elevation
is basically achieved by the overexpression of the CK biosynthetic gene;
ISOPENTENYL TRANSFERASE, which improves root growth that en-
hances the antioxidant system activity and hence increases drought
tolerance (Xu et al., 2016). During drought stress, plant shows a sig-
nicant accumulation of CK in root tissues due to a decrease in the ac-
tivity of CYTOKININ OXIDASE/DEHYDROGENASE (Havlov´
a et al.,
2008). The down-regulation of CK has been mostly accomplished by
overexpression of CYTOKININ OXIDASE/DEHYDROGENASE that is
shown to elevates the content of protective compounds and slows the
plant growth rate, which ultimately leads to increased drought tolerance
in Arabidopsis, tobacco, and barley (Mackov´
a et al., 2013; Nishiyama
et al., 2011; Pospíˇ
silov´
a et al., 2016). CK works in several ways to
activate signaling in response to drought stress. The elevation of CK
concentration during stress, and activation of stress-responsive genes
could provide several clues to nd a potential target to make plants more
tolerant of drought stress. Several secretory proteins and antioxidants
are regulated by CK and could be a future target to improve drought
resistant plants.
3.4. Ethylene
Ethylene is another signicant plant growth regulator, which plays a
prominent role in ameliorating the harmful impact of abiotic stress
conditions, as well as, plays a signicant role in fruit softening (Pech
et al., 2018; Wang et al., 2020). ET is a simple two-carbon structure
synthesized from methionine through S-adenosyl-L-methionine 1-ami-
nocyclopropane-1-carboxylic acid (cyclic, nonprotein amino acid)
(Vandenbussche and Van Der Straeten, 2018). It is demonstrated that ET
has been found to play a signicant role in the initiation of autophagy
and induction of ROS amelioration and thereby promotes survival dur-
ing reoxygenation stress, ooding, and hypoxia (Hartman et al., 2020).
Further, the ET signaling pathway is involved in systemic resistance in
Arabidopsis, mediated via the plant growth-promoting fungus Penicil-
lium viridicatum (Hossain et al., 2017). ET founds to play a key role in
nodule formation and nodule signaling in response to a diverse range of
biotic and abiotic stresses (Khalid et al., 2017). Furthermore, it promotes
nodal root emergence that causes retardation in nodal root development
and ultimately leads to a negative effect on root-lodging resistance in
Zea mays (Shi et al., 2019). The studies showed that ET controls
adventitious root initiation sites in Arabidopsis hypocotyls (Rasmussen
et al., 2017). The exogenous application of phytohormones like ABA and
ET induces the expression of AtNIP5;1, which further enhances boron
uptake in Arabidopsis (G´
omez-Soto et al., 2019).
The overexpression of GmERF3, causes enhancement in the soluble
sugar, proline content, and reduction in the accumulation of malon-
dialdehyde to improve drought tolerance in the tobacco plant (Zhai
et al., 2017). Further, SlERF5 over-expressing transgenic tomato plants
exhibited high tolerance against drought (Pan et al., 2012). 269 AP2/
EREBP genes were reported in cotton and known to respond to water
stress (Liu and Zhang, 2017). Like other phytohormones, ET also regu-
lates several signaling for drought management. So, the above infor-
mation on ET-mediated stress responsive gene could be of interest to the
future studies.
3.5. Gibberellins
Gibberellins are the class of diterpenoid phytohormone having an
ent-gibberellane ring structure, which contains 19 or 20 carbon atoms.
These GA are synthesized from geranylgeranyl diphosphate via terpenes
route and feature a fundamental structure constructed by an ent-
gibberellin tetracyclic skeleton (Olszewski et al., 2002). Based on the
enzyme involved, the biosynthetic pathway is divided into three stages.
In the rst step, ent-kaurene is synthesized in plastids by soluble en-
zymes. While in the second step, the end product of the rst step is
oxidized by microsomal MONOOXYGENASES, and in the third step, the
reaction is catalyzed by 2-OXOGLUTARATE-DEPENDENT DIOXYGE-
NASES. GA consists of a large family of phytohormones that were
discovered in the 1930s in Japan. It acts as a growth regulator, especially
for seed germination, stem elongation, increasing fruit size, and causes
the induction of owering (Camara et al., 2018). GA was found to
regulate vegetative and reproductive growth of Hibiscus cannabinus L., as
well as improves its ber property (Muniandi et al., 2018). Exogenous
application of GA enhances the number of fertile seeds, antioxidant SOD
activity, increase in individual fruit weight, and delay in fruit ripening
time without affecting the fruit shape of rabbiteye blueberry (Vaccinium
ashei) (Zang et al., 2016). Further, this phytohormone was reported to
enhance the sucrose and dry matter content in sugarcane (Rai et al.,
2017). Also, it has been reported to increase plant fresh and dry weight,
tiller number, and height of Leymus chinensis and Cichorium intybus in
both pot and eld conditions (Ma et al., 2018). GA-treatment is shown to
promote early sprouting and a large number of sprouted bud formation
in potato tuber (Alexopoulos et al., 2017).
In addition, GA reduces the zinc accumulation and reactive oxygen
species generation, caused by zinc oxide nanoparticle stress in wheat.
Further, it improves nutrient quality, photosynthesis, biomass, and yield
of wheat plants (Iftikhar et al., 2019). Exogenous application of GA in-
duces the up-regulation of lipid biosynthesis in salt-stressed rice (Liu
et al., 2018). GA application enhances H
2
S production (the downstream
molecular signal), which acts as an antioxidant to reverse oxidative
stress, increase plant growth, reduces the boron content (Kaya et al.,
2020). It improves tolerance for temperature stress by altering the cell
wall and plastid structure in Solanum lycopersicum L. (Gamel et al.,
2017). Exogenous application of 0.1 mM GA along with 0.1 mM ascorbic
acid reduces the toxic effect of saline stress in okra by increasing con-
centration of macro-elements (K, Ca, Mg and Fe) and osmoprotectants
(proline and soluble protein), which stimulates antioxidant enzymes,
and decreasing H
2
O
2
content, lipid peroxidation and electrolyte leakage
(Wang et al., 2019a, 2019b, 2019c). Also, the application of 10
-6
M of
GA on tomato was shown to enhance solute like sugar and proline in the
cytosol, which acts as an osmoprotectant and improves various growth
parameters under 100 mM salt stress condition (Ben Rhouma et al.,
2020).
Chhaya et al.
Plant Gene 25 (2021) 100264
6
Reduced GA levels have been reported to enhance drought tolerance
in plants via suppressing plant growth (Wang et al., 2012). The over-
expression of AtGAMT1 gene generates inactive GA by encoding an
enzyme that promotes the methylation of active GA. Transgenic plants
with the lower GA level tend to produce smaller leaves, with high sto-
matal intensity and lower stomatal conductance, which reduces the
transpiration rate (Nir et al., 2014). Further, the overexpression of
SlDREB downregulates GA biosynthetic genes. Lower GA level promotes
the drought tolerance mechanism in tomatoes by restricting internode
elongation and leaf expansion (Li et al., 2012). Moreover, the over-
expression of PtGA2ox1 decreases the GA level in the roots, stems, and
leaves of the tobacco plant to promote drought tolerance (Zhong et al.,
2014). So, we conclude that GA negatively regulated the drought stress
in plants in contrast to other phytohormones. So the downregulation of
GA could be a major target to make drought-tolerant plants.
3.6. Brassinosteroids
Brassinosteroids are the group of polyhydroxylated sterol derivative
phytohormones present in all plant species. BRs show structural simi-
larity to that of animal steroidal hormones. It was rst isolated from
Brassica napus pollen (Saini et al., 2015). Endogenous BRs may synthe-
size close to the site of action (Bishop and Yokota, 2001). The BRs level
varies across the tissue age, species, and plant organ type. Immature
seeds, young growing shoots, and pollen contain a higher level of BRs
than the mature tissues (Clouse, 2011). BRs are biosynthesized from 24-
methylenelophenol via sterol biosynthetic pathways (Du et al., 2017).
This phytohormone plays an essential role in the growth and develop-
ment of plants and response to stress conditions. BRs are not only related
to root elongation, but it also involved in several aspects of root devel-
opment, including maintenance of meristem size, gravitropic response,
lateral root initiation, root hair formation, mycorrhiza, and nodule
formation (McGuiness et al., 2019; Wei and Li, 2016). BRs signaling
contributes resistance against freezing stress and improves cold accli-
mation (Landrein et al., 2018). It is reported that BRs and H
2
O
2
regulate
guard cell starch metabolism and stomata opening (Li et al., 2020). It
also provides a protective role under pesticide stress (Sharma et al.,
2018). BRs activated transcription factor BRASSINAZOLE-RESISTANT1
(BZR1) accumulates at a high temperature, which further binds to the
promoter of PIF4, where it induces the expression of several growth-
promoting genes (Iba˜
nez et al., 2018). Over-expression of OsMIR396d
affects BRs and GA signaling to regulate plant architecture in Oryza
sativa and also affects plant yield potential (Tang et al., 2018). Oryza
sativa mediator subunit 25 is a signicant regulator of BRs signaling,
which interacts with OsBZR1 to monitor plant architecture and BRs
signaling in rice (Ren et al., 2020). BRs-associated H
+
efux is critical in
the root hydrotropism response in Arabidopsis (Miao et al., 2018). In
addition, the BZR1 activates the transcripts of autophagy-related genes,
which further induces autophagy and nitrogen starvation in Solanum
lycopersicum (Wang et al., 2019a, 2019b, 2019c).
BRs improve the CO
2
assimilation and leaf water economy by
inducing Rubisco and water use efciency of leaves during water stress
(Farooq et al., 2009a). Several studies have also suggested the positive
role of BRs in Brassica napus, Arabidopsis, and wheat during drought
stress (Kagale et al., 2007; Sairam, 1994). The exogenous application of
24-epibrassinolide increases the BRs content and decreases ABA and
ROS levels, which further helps to increase the stomatal aperture during
drought resistance (Nie et al., 2019; Tanveer et al., 2019). More
recently, three WRKY transcription factors (WRKY46, WRKY54, and
WRKY70) have been reported as the important signaling elements that
positively and negatively participate in BRs regulated growth and in
drought responses, respectively (Chen et al., 2017). Similarly, the
overexpression of BRs biosynthetic gene AtDWF4 from Arabidopsis in
Brassica napus results in enhanced drought tolerance (Sahni et al., 2016).
Further, ABI1 and ABI2 negatively regulate ABA signaling, which was
reported to interact with BIN2 and regulates BRs signaling, which
ultimately shows stress responses in Arabidopsis (Wang et al., 2018a,
2018b). BRs are a local hormone that plays a crucial role in drought
stress by involving other important stress hormones like ABA.
3.7. Jasmonate
Jasmonate is 3-oxo-2-2′-cis-pentenyl-cyclopentane-1-acetic acid, a
ubiquitous plant signaling compounds derived from
α
-linolenic acid. Its
biosynthesis requires three different sites viz. chloroplast, peroxisome,
and cytoplasm. JAs are generally produced in owers. The unsaturated
fatty acid is converted to deoxymethylated vegetable dienic acid or 12-
oxo-phytodienoic acid in the chloroplast. Further, it converted to JA in
peroxisomes, which was nally metabolized to several structures via a
diverse chemical reaction in the cytoplasm (Ruan et al., 2019). JA en-
hances root growth, tendril coiling, viable pollen production, and fruit
ripening (Delker et al., 2006; Wasternack, 2007). Exogenous application
of JA proposed to increase antioxidant activity via induction of MON-
ODEHYDROASCORBATE REDUCTASE, DEHYDROASCORBATE REDUC-
TASE, GLUTATHIONE REDUCTASE, and ASCORBATE PEROXIDASE
during drought stress (Shan et al., 2015). Furthermore, it has been re-
ported to promote plant water uptake by modulating root hydraulic
conductivity in limited moisture conditions (S´
anchez-Romera et al.,
2014).
Methyl JA plays an important role in promoting photosynthetic rate,
grain yield, and drought tolerance in several crops, including maize,
soybean, banana, and Cistus albidus (Anjum et al., 2016; Yu et al., 2019).
Moreover, methyl JA promotes enhanced accumulation of compatible
solutes and osmoprotectants to enhance the antioxidant activity, chlo-
rophyll content, and leaf gas exchange to induce stomatal closure to
improve water-use efciency and water status. It also changes poly-
amine and endogenous phytohormones to alleviate the damaging effects
of drought stress (Xiong et al., 2020).
Exogenous application of 0.5 mM methyl JA is reported to maintain
wheat growth and yield during drought stress (Anjum et al., 2016).
Further, 10
μ
M of methyl JA application reduces the severe drought
effects in sugar beet (Fugate et al., 2018). A high concentration of
methyl JA up to 20
μ
M modulates diverse physiological responses such
as increased solutes and secondary metabolites content, including a-
vonoids and phenolic compounds, improving plant growth under
drought stress (Mohamed and Latif, 2017). We conclude that JA
signaling is associated with secondary metabolite regulation for drought
management in plants.
3.8. Salicylates
Salicylates, an ortho-hydroxyl benzoic acid, is one of many phenolic
compounds comprising a benzene ring carrying one or more hydroxyl
groups. It is synthesized in the chloroplast (Dempsey and Klessig, 2017).
SA is a phytohormone that is biosynthesized from the chorismate via two
different and independent pathways; phenylalanine ammonia-lyase and
isochorismate synthase dependent pathways (Dempsey and Klessig,
2017). Increasing SA in plants suggests its critical role in regulating
plant disease resistance, abiotic stress tolerance, thermogenesis, seed
germination, fruit yield, DNA damage/repair, etc. (Dempsey and Kles-
sig, 2017). Around a 20-fold increase in endogenous SA has been re-
ported in tobacco in response to the tobacco mosaic virus to provide
resistance to disease (Klessig et al., 2018). Exogenous SA application
showed increased enzymatic activity, which modulates the cell redox
balance, protects the plants from oxidative damage, and reduces the
negative effect in a mustard plant under salt stress (Husen et al., 2018).
SA is also involved in cell expansion, cell division, and its exogenous
application on canola results in an increase in the number of pods and
seed yield (Keshavarz and Sanavy, 2018). Moreover, its application on
marigold under drought stress increases bio productivity, improves
various physiological processes as well as ameliorates the negative
impact of water stress (Abbas et al., 2019). In addition, SA stimulates
Chhaya et al.
Plant Gene 25 (2021) 100264
7
proline content and antioxidant enzymes, which is very critical in alle-
viating aluminum stress in mung bean seedlings (Ali, 2017). Further,
exogenous application of SA ameliorates the growth and yield of maize,
strawberry, and other economically important crops under salinity
stress (Faghih et al., 2017; Tahjib-Ul-Arif et al., 2018). The SA is also
found to maintain the glutathione level and redox homeostasis in salt
stress conditions (Csisz´
ar et al., 2018).
SA application is reported to elevate osmolyte and proline content in
root and shoot to maintain the turgor pressure of cell without interfering
with the other metabolic process. Its application activates non-
enzymatic defense processes like sugar accumulation for energy con-
servation and osmoregulation, and reduces the free radical and
Figure 3. Diagrammatic representation of recent techniques and mechanisms used to improve crop plants towards drought tolerance. Exogenous and endogenous
modication, production, and application of phytohormones are the major methods to improve plants against drought stress tolerance.
Figure 4. Diagrammatic representation showing various gene regulatory pathways associated with drought stress management in plants. These pathways include
upregulation of genes (green colored boxes), downregulation of genes (yellow-colored boxes), and negative regulation of genes (pink colored boxes). All these
different types of gene regulation pathways ultimately lead to making drought-tolerant plants.
Chhaya et al.
Plant Gene 25 (2021) 100264
8
malondialdehyde content in several crop plants, such as wheat, saf-
ower, and Brassica rapa during drought stress (Chavoushi et al., 2019;
Ilyas et al., 2017). SA application enhances the drought-stress tolerance
through redox homeostasis and proline metabolism in crop plants
(Chavoushi et al., 2019; Ilyas et al., 2017; La et al., 2019). The Arabi-
dopsis loss of function lines, cpr5 and acd6 exhibited a drought tolerance
mechanism by endogenously accumulated SA (Miura et al., 2013).
CAPIP2 gene from the pepper that is expressed during pathogen infec-
tion, when introduced to Arabidopsis, showed increased tolerance to
several abiotic and biotic stresses, including drought (Lee et al., 2006).
Furthermore, SIZ1 - mediated accumulation of endogenous SA was re-
ported to enhance drought tolerance and promote stomatal closure in
Arabidopsis (Miura et al., 2013).
Exogenous application of SA was assessed to improve drought
tolerance by activating several defense pathways such as the antioxidant
system and increasing osmolyte content in the vegetative phase of saf-
ower, corn, and barley, respectively (Abdelaal et al., 2020; Bijanzadeh
et al., 2019; Chavoushi et al., 2019). So, targeting genes involved in
signaling in response to the exogenous application of SA could be a
potential target for transgenics in order to make drought resistant plants.
4. Conclusion and prospective
Drought stress intensively reduces the yield by affecting the growth
and development of plants. The ever-increasing world population is
compelling the researchers to develop a more efcient approach for
augmenting crop yield to ensure food security under such water stress
conditions. To date, several remarkable studies show the importance of
phytohormones in drought stress management. The information pro-
vided in the current review focuses on phytohormones and their role in
drought stress. Phytohormones, such as ABA, JA, SA, GA, CK, BRs, ET,
and auxins, regulate several biological processes associated with
drought stress. Up or downregulation of these phytohormone-associated
genes regulate an extensive array of responses to drought stress. Ectopic
overexpression of various genes indeed takes part in several phytohor-
mones’ biosynthesis, evidently involved in drought stress tolerance by
mediating different biosynthetic pathways. To cope with the drought
stress, several techniques, including engineered genes responsible for
endogenous phytohormone synthesis and its exogenous application, are
mainly used to maintain and improve productivity, as shown in Figure 3.
Figure 4 represents some of the gene regulatory pathways in drought
stress. Table 2 represents some recent work to improve drought toler-
ance in some major crops. However, there is much more work remains
elusive in the eld of drought stress. Possible outcomes in this eld could
be the development of drought-tolerant varieties through genetic ma-
nipulations should be applied in all major crops. Various plant growth-
promoting microbes enhance drought resistance in numerous plant
species by altering endogenous phytohormone, secondary metabolite,
and several osmoprotectants. This interaction could be a low-cost and
environment-friendly technology and has a high probability of crop
improvement. Further, the exogenous chitosan and spermine applica-
tions are associated with endogenous phytohormone changes, reported
to enhance drought tolerance. So, in a nutshell, genetic engineering and
gene manipulation of drought-responsive genes could assist in
enhancing the drought resistance ability of plants.
Author contributions
OPN has conceptualized the theme of this review. C, BY, AJ, and OPN
have written and compiled the original draft including gures and ta-
bles. C, BY, PG, PK, NL, SKL, JP, and OPN have reviewed & edited the
manuscript. All authors nally read and approved the manuscript.
Declaration of Competing Interest
The author declares no conict of interest.
Acknowledgments
We acknowledge the Indian Council of Agricultural Research (ICAR),
Council of Scientic and Industrial Research (CSIR), Tufts University,
Boston, USA, Jawaharlal Nehru University, New Delhi, India. We also
acknowledge the nancial support received from the Council of Scien-
tic and Industrial Research (CSIR).
Table 2
List of recently modied phytohormones-mediated drought-tolerant major crop
plants.
SN Crops Modication Trait Reference
1. Rice Overexpressing
OsbZIP42
Elevated expression of
the ABA-responsive
LEA3 and Rab16 genes
(Joo et al., 2019)
2. Rice Ectopic expression
of specic GA 2
oxidase mutants
Moderately lowered
GA level
(Lo et al., 2017)
3. Rice Overexpression of
OsJAZ1
Regulates JA and ABA
signaling
(Fu et al., 2017)
4. Rice Expression of
OsERF109
By affecting the
ethylene biosynthesis
(Yu et al., 2017)
5. Rice Over-expressing
OsSAP
Maintain a level of
phytohormones ABA,
JA, indole-3-
carboxylic acid, GA,
and zeatin
(Ubaidillah
et al., 2016)
6. Wheat Rhizobacteria Increase IAA, reduce
ABA
(Barnawal et al.,
2017)
7. Wheat Exogenous
application of SA
Diminish diverse
effects of drought in
plants
(Sarvestani
et al., 2017)
8. Wheat Pre-drought
priming
Increase IAA, GA, and
lower ABA content in
grains
(Abid et al.,
2017)
9. Wheat 24-epibrassinolide
pretreatment
Accumulates ABA and
decreases indoleacetic
acid and CK
(Shakirova et al.,
2016)
10. Maize 24-Epibrassinolide
and/or spermine
application
Altering
phytohormones prole
(Talaat, 2020)
11. Maize Endophytic fungus Stimulated genes for
phytohormone
functions
(Zhang et al.,
2018)
12. Maize Exogenously
applied spermidine
Increases endogenous
IAA and GA A3 and
decreased SA and JA
(Li et al., 2018)
13. Maize Melatonin
applications
Signaling function
about the stress-
related
phytohormones (ABA,
SA, and JA)
(Fleta-Soriano
et al., 2017;
Sharma and
Zheng, 2019;
Sharma et al.,
2020)
14. Maize l-tryptophan-
assisted
Pseudomonas sp.
Higher
phytohormones
including IAA and GA
in leaves and soil
(Yasmin et al.,
2017)
15. Maize Mitsuaria sp.
ADR17 and
Burkholderia sp.
ADR10
Decreases plant
ethylene levels and
changes other
phytohormone content
(Huang et al.,
2017)
16. Barley Exogenous SA Enhances
accumulation of K
+
,
Ca
++
in shoot and root
and K
+
, Ca
++
and
Mg
++
in three organs
(El-Samad et al.,
2019)
17. Barley Brassinosteroid
Mutants
Accumulates JA, ABA,
and SA
(Gruszka et al.,
2016)
18. Barley Overexpressing
cytokinin
dehydrogenase 1
Changes
phytohormones
concentration (IAA,
JA, and CK)
(Vojta et al.,
2016)
Chhaya et al.
Plant Gene 25 (2021) 100264
9
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