2. 11.1 Introductio 255
cues are those intermediate compounds synthesized via plant biosynthetic pathway that
act locally on the site of synthesis or may be transported elsewhere in the plant. These
chemical messengers are collectively termed as phytohormones and regulate various
aspects of plant growth, development, and stress (biotic and abiotic stresses) adaptive
responses. Almost each and every phase of development of plant from cell division, expan-
sion, differentiation, embryogenesis to senescence is said to be controlled by phytohor-
mones. Other diverse actions, namely seed germination, defining plant architecture,
flowering response, ripening and shedding times, and apical, basal, and radial growths, are
regulated through these hormones (Peleg and Blumwald 2011). Studies have indicated that
these stressful conditions sometimes transduce a significant role in governing plant
response toward stress, again mediated by downstream hormonal signaling pathways
(Teale et al. 2008). Phytohormones, mainly auxins, cytokinins (CKs), and gibberellins
(GAs), and a gaseous hormone ethylene (ET) are reported as classical plant hormones and
are primary signals that govern growth and development, whereas abscisic acid (ABA),
brassinosteroids (BRs), jasmonic acid (JA), salicylic acid (SA), and strigolactones (SLs) are
categorized as class of new phytohormones having a prominent role in plant defense and
mitigating biotic and abiotic stresses in plants (Lorenzo and Solano 2005; Mauch-Mani and
Mauch 2005).
The major advancement achieved in the area of phytohormones and their respective
response is the identification of precise receptor for majorly known hormones. These
chemical messengers are translocated to several organelles where they bind to their target
site via receptor-mediated recognition and further transduce the signal downstream by
themselves getting degraded. Thus, ordered degradation of protein also plays a pivotal role
in hormone signaling, which is regulated mainly by ubiquitin-mediated degradation
(Santner et al. 2009). Several synergistic or antagonistic actions take place simultaneously,
which are primarily key to regulation of defense mechanism in plants against variety of
stresses, and termed as signaling cross talk. In the recent research, efforts have been laid
down to reveal the complex physiological and molecular responses of stress tolerance,
however the molecular intricacy still remains ambiguous. The major problem lies in the
complex nature of plant response for different situations, as both biotic as well as abiotic
stresses are known to express extreme yet similar suites of genes. A common factor for both
types of stress is said to be the generation of small molecules, which, if not regulated, are
known to be highly toxic at higher concentration and are termed as active or reactive oxy-
gen species (ROS). The generation and simultaneous scavenging of ROS holds a key step
involved in response to biotic and abiotic stresses (Apel and Hirt 2004). Using large scale
transcriptome and microarray analysis, it is evident that similar cross talk exists between
these signaling networks (Seki et al. 2002; Cheong et al. 2002; Davletova et al. 2005). The
evidence that ROS may act as a common downstream messenger for transducing multiple
stress signals was established in plants challenged either with heavy metal or with necro-
trophic pathogen where a similar increase in ROS levels was monitored. The study demon-
strated a similar yet overlapping set of responses in all plants challenged with either type of
stress. Apart from their role in growth enhancement, an improved plant growth and yield
was observed through exogenous application of phytohormones. In a study, Li et al. (2012)
reported an increased photosynthetic activity, enhanced nitrogen metabolism, and
improved generation of amino acid through application of brassinosteroid hormones in
3. 11 Role of Growth Regulators and Phytohormones in Overcoming Environmental Stress
256
Camellia sinensis. The authors further reported an improved hormone metabolism as well
as better antioxidant system in maize seedlings primed with exogenous salicylic acid and
H2O2, thus helping maize seed to mitigate deleterious effects of chilling stress. Recent study
conducted by Singh et al. (2017) reported active involvement of multiple stress hormones,
namely brassinosteroids, salicylic acids, and jasmonic acids under several environmental
stresses.
The present chapter is an effort to summarize the notion that phytohormones mediate a
complex set of signaling pathways having frequent cross talk in different levels of hormo-
nal responses, thereby allowing plants to mitigate environmental stress.
11.2
Function of Classical Plant Hormones in Stress Mitigation
11.2.1 Auxins
Auxin happens to be the first plant hormone discovered where the major productive sites
in plants are the shoot apex and young buds and the major movement is known to be polar
from apex to the base of organ. Indole acetic acid (IAA), a natural auxin, is a major player
for growth regulation in plants such as vascular development, initiation of cell elongation,
and apical dominance (Wang et al. 2001). Apart from their major role in development,
several diverse reports also justify their role in salt stress alleviation. Ribaut and Pilet (1994)
reported varying levels of IAA, that were found similar to the level of abscisic acid (also
known for growth retardation), thus relating this increased IAA level to the significant
decline observed in plant growth and supposed this to be mediated by abscisic acid. They
reported that the growth reduction under environmental stresses was due to an altered
level of auxins, especially IAA. Hence, exogenous application of plant hormones could be
one of the approaches to counter the deleterious effects of environmental stress. Similar
results were obtained by Prakash and Prathapasenan (1990), where NaCl treatment resulted
in a significant decline in IAA in rice leaves, interestingly this effect was said to be reversed
by applying exogenous gibberellic acid in rice leaves. Similarly, salt stress was able to cause
a reduction of 75% in IAA levels in tomato plants (Dunlap and Binzel 1996). In addition,
Sakhabutdinova et al. (2003) indicated that salt stress negatively affects the root system of
plants, as recorded by monitoring a continuous decline in IAA levels under stress. Akbari
et al. (2007) demonstrated an increase in hypocotyl length, fresh weight, and dry weight of
wheat seedlings supplemented with exogenous auxin during salt stress condition.
Additionally, presoaking of wheat seeds in IAA was reported to alleviate the inhibitory
effect of salinity stress (Sastry and Shekhawat 2001; Afzal et al. 2005). Apart from their role
under abiotic stress, endogenous IAA levels are reported to augment in plants challenged
with biotic stress specifically for pathogen infections (O’donnell et al. 2003). Repression in
auxin signaling also leads to enhanced antibacterial resistance, which again corroborates
that auxin imparts a key role in modulating plant responses under pathogenesis
(Navarro et al. 2006).
At molecular level, auxin is reported to influence the transcription of various down-
stream genes termed as primary auxin-responsive genes mainly classified into three differ-
ent gene families, of them auxin/indole acetic acid (Aux/IAA) is a primary gene family,
4. 11.2 Function of Classical Plant Hormones in Stress Mitigatio 257
which is followed by GH3 gene family, and the third is small auxin up-regulated RNA
(SAUR) gene family (Guilfoyle et al. 1993). Members belonging to Aux/IAA gene family are
primarily recognized in light-mediated regulation of auxin responses (Berleth et al. 2004).
GH3 gene family is basically characterized and validated by generating various mutants
having altered gene expression. In a related study, GH3-overexpressing mutants exhibited
retarded growth and altered response toward light signaling, which further confirms the
role of these GH3 proteins in light–auxin interactions. Proteins of SAUR family are known
to bind to calcium/calmodulin (Yang and Poovaiah 2000), suggesting that calcium ions are
vital for auxin signaling. Members of the Aux/IAA gene family have been mostly identified
and characterized from members of rice, Arabidopsis, and soybean species (Hagen and
Guilfoyle 2002), and this association of auxin gene family members with calcium and light
determines them as being regulators of stress signaling. Therefore, from the literature it
becomes evident that auxin, a key player for apical dominance, also plays a major role
under stressful conditions governing multiple physiological, morphological, and develop-
mental genes downstream.
11.2.2 Cytokinins
Cytokinins are phytohormones having the ability to promote plant cell division and con-
trolling many developmental practices such as cell division, chloroplast biogenesis, vascu-
lar differentiation, shoot differentiation, retarding senescence, and to some extent pigment
production (Davies 2004). Cytokinins are majorly produced in the tip of roots and in seeds
of developing stage and translocated to shoots via xylem, thereby regulating processes,
namely growth, development, and senescence (Zahir et al. 2001). Apart from their roles in
morphological developments, several reports elucidate their role in mitigating abiotic
stress-induced damage in plants (Barciszewski et al. 2000). Studying various developmen-
tal processes in plants reveals cytokinin to behave as antagonists/synergists for other stress
hormones, namely ABA and auxins (Pospíšilová 2003). Therefore, in contrast to ABA treat-
ment, seed priming with cytokinins is said to enhance stress tolerance for treated seeds
such as gibberellins (Iqbal et al. 2006). Release of stress-induced dormancy via application
of kinetin, a cytokinin, is reported in germination studies conducted using seeds of tomato,
barley, and cotton (Bozcuk 1981). Furthermore, Boucaud and Ungar (1976) demonstrated
an increased growth of chickpea seedlings through exogenous application of kinetin.
Similarly, kinetin treatment was found to be helpful in countering effect of salinity stress
on wheat seedling growth (Naqvi et al. 1982). Moreover, treatment of kinetin before salt
treatment was also found helpful in ameliorating salinity stress-induced growth inhibition
(Abdullah and Ahmad 1990). In a field study, increased rice yield, up to 45.8%, was obtained
through cytokinin application under stress when compared to control rice plants subjected
to similar stress (Zahir et al. 2001). Chakrabarti and Mukherji (2003) hypothesized that this
stress alleviation may be due to the protective role of kinetin or in altering the antioxidant
defense mechanism, which is helpful in protecting the purine breakdown. Cytokinin sign-
aling is designated as two-component signaling system demonstrating close similarity to
bacterial system (To and Kieber 2008). Cytokinin is perceived by a membrane-bound
kinase receptor that transfers phosphate group to a protein named arabidopsis his
phosphotransfer (AHP) protein. These proteins subsequently phosphorylate downstream
5. 11 Role of Growth Regulators and Phytohormones in Overcoming Environmental Stress
258
protein machinery termed as arabidopsis response regulator (ARR) protein, which is a
nuclear located protein either positively or negatively regulated. Cytokinins are thus asso-
ciated to be regulating pool of transcription factors termed as cytokinin response factors,
which after treatment are able to regulate a large number of genes downstream (Peng et al.
2008; Rashotte et al. 2003). Functional analysis of receptors of cytokinins in a model crop
Arabidopsis thaliana revealed the presence of three different cytokinin receptors and fur-
ther studies indicated them as negative regulators of ABA signaling in relation to osmotic
stress (Tran et al. 2007). However, characterization of similar receptors in other plant spe-
cies showed them to be governed by external osmotic surroundings, which also signify
their role under osmotic stress response (Merchan et al. 2007). Thus, above mentioned
reports clearly suggest the vital role of this hormone in promoting growth under stressful
conditions.
11.2.3 Gibberellins
GAs are known to play numerous physiological roles including growth and overall devel-
opment in plants. They are known to regulate germination of seeds, expansion of leaves,
metabolizing starch, elongation of cell and stem, and also involved in regulating flowering
(Magome et al. 2004). More than a hundred types of gibberellins have been studied and
characterized showing diverse roles. The GAs known for cell elongation show complete
diversity from the GAs known for enzyme synthesis, as proven by studies done in barley
plants (Grobelindemann et al. 1991; Banerjee and Roychoudhury 2019). GA biosynthesis is
regulated by developmental as well as environmental stimuli (Yamaguchi and Kamiya
2000; Olszewski et al. 2002). GA levels are known to fluctuate and influenced by actions of
the other hormones, namely auxin and ethylene (Yamaguchi 2008). Gibberellic acid is also
known to accumulate rapidly in plants imposed with either biotic (McConn et al. 1997) or
abiotic stress (Lehmann et al. 1995). Several phytohormones have been used for alleviating
deleterious effects of salinity; among them gibberellins have been given the foremost
importance (Basalah and Mohammad 1999; Hisamatsu et al. 2000). Studies relate the vital
role of gibberellins under stress, as evident by a report where application of gibberellin
resulted in enhanced growth of wheat and rice under salinity stress (Parashar and Varma
1988; Prakash and Prathapasenan 1990). An important breakthrough came when a nega-
tive regulator of gibberellins was identified and reported. Reports hypothesized the role of
a protein termed as DELLA protein, which works as a negative regulator of GA response.
The GAs were known to promote the degradation of DELLA proteins. The name DELLA is
attributed for N-terminal DELLA domain and presence of a DELLA motif (aspartate-glu-
tamate-leucine-leucine-alanine) or D-E-L-L-A in the single letter amino acid code which is
conserved and also includes a C-terminal GRAS domain (Schwechheimer 2008). GRAS
proteins are an important family of plant-specific proteins named after the first three mem-
bers: gibberellic-acid insensitive (GAI), repressor of GAI (RGA) and Scarecrow (SCR).
Reports indicated that DELLA proteins are also responsible for abiotic stress-induced
growth retardation in plants (Achard et al. 2006; Magome et al. 2004). DELLA also medi-
ates inhibition of cell elongation via binding to the DNA-binding domain of transcription
factors, namely phytochrome interacting factor3 (PIF3), PIF4, and PIF5. Binding subse-
quently refrains these PIF transcription factors to bind with promoters of growth of specific
6. 11.2 Function of Classical Plant Hormones in Stress Mitigatio 259
genes, thus indirectly stimulating their transcription (Feng et al. 2008; De Lucas et al.
2008). These results were further corroborated in a study performed in phytochrome-
overexpressing transgenic tomato plants, which showed significant similarity to GA
mutants in terms of growth (Boylan and Quail 1989; Koornneef et al. 1990). Substantial
evidences regarding phytochrome-A-mediated modulation in GA level were postulated by
Jordan et al. (1995), where overexpression of phytochrome-A resulted in production of
shorter tobacco plants. Concluding evidences state that GAs promote destabilization of
DELLA proteins, which is modulated by salt and light also including hormone signaling
(auxin and ethylene respectively). This substantiates the hypothesis that a cross talk does
exist at the molecular level (Achard et al. 2006). Further studies in model crop A. thaliana
also govern stress response via modulating plant antioxidant system through DELLA-
mediated transcriptional regulation (Achard et al. 2008). DELLA activity prevented an
increased load of generation of ROS in plants, which are a known by-product generated
under different environmental stresses. ROS is known to trigger plant cell death at higher
levels, however this response is said to be delayed by DELLA (Achard et al. 2008; Colebrook
et al. 2014). In an attempt to study seed priming using GAs, the authors reported an
increased yield of grain in wheat, where GA priming was said to modulate the ion uptake
and ion partitioning inside shoots and roots, thereby improving hormone homeostasis and
photosynthesis under saline conditions (Iqbal and Ashraf 2013). The results show that
modulation of GAs and its optimized usage could impart better salinity tolerance for the
crops grown under saline conditions.
11.2.4 Ethylene
Ethylene is a gaseous hydrocarbon produced in small quantities in plants and has a special
role as a phytohormone that is effective mostly in the range 0.01–10μl. Ethylene, a natural
product of plant metabolism, was postulated early in 1935. Ethylene is synthesized in tis-
sues undergoing senescence or ripening and is also termed as a fruit-ripening hormone,
however in various tissues this is also produced in response to stress. Ethylene levels tend
to increase sharply in fruits such as apples and tomatoes, which further augment the spe-
cific ripening processes, namely chlorophyll breakdown, increased respiration, breakdown
of cell wall and sugars, and synthesis of aromatic compounds and pigments. Under envi-
ronmental stresses, plants often exhibit similar symptoms such as exposure to ethylene.
Studies indicated this effect to be derived through induction of an ethylene biosynthesis
precursor, 1-aminocyclopropane-1-carboxylic acid (ACC), which serves as an intermediate
and results in generating ethylene-like symptoms (Hyodo et al. 1991). Ethylene biosynthe-
sis under stress is regulated through de novo synthesis of ACC synthase, which is responsi-
ble for regulating its own transcription under stress (Morgan and Drew 1997; Hyodo et al.
1991). Reports suggest that cumulative effect of multiple stresses augments ethylene bio-
synthesis, thus perturbing the ethylene-synthesizing enzymes that directly correlate to
decline in water potential further increasing the severity of stress-induced damage (Abeles
1992). The complexities of drought and temperature stresses were monitored using soy-
bean plants where a mild drought was not able to trigger ethylene production or modulate
the ACC levels, while a severe drought augmented both the parameters simultaneously
(Chang-cheng and Qi 1993). Similarly, leaf membrane damaged with dry air was also able
7. 11 Role of Growth Regulators and Phytohormones in Overcoming Environmental Stress
260
to increase ethylene production and elevated the level of ACC (Chang-cheng and Qi 1993).
Several reports extend this cross talk of ethylene production in regulating abscisic acid
levels, where elongated primary roots were observed in maize seedlings under drought
stress. The effect was correlated with increased ABA level recorded in root tips, which was
due to elevated ethylene levels under drought stress (Spollen et al. 2000). Induction of eth-
ylene-like symptoms under stress was quite apparent and revealed a complex interplay of
biosynthetic pathway and ethylene sensitivity.
11.3
Role of Specialized Stress-responsive Hormones
11.3.1 Abscisic Acid
ABA, another vital hormone, holds a critical role in regulating environmental stresses
transducing the signal further downstream. ABA is produced primarily in roots and slightly
matured leaves, in response to stress caused by lack of water from glyceraldehyde 3-phos-
phate through isopentenyl diphosphate and carotenoids. Its foremost roles include regula-
tion of stomata, morphogenesis of embryo, leaf senescence, and synthesis of stored proteins
and lipids (Roychoudhury and Paul 2012). Other adaptations, namely drought, low tem-
perature, and salinity, are mostly governed through two separate yet overlapping pathways,
namely ABA-dependent and ABA-independent signaling pathways. Several proteins such
as stress-inducible transcription factors having a proven role in stress acclimation are
known to regulate ABA signaling downstream; these include specific transcription factors,
namely DREB2A/2B, AREB1, RD22BP1, and MYC/MYB (Roychoudhury et al. 2013). All
these have proven roles in regulating ABA-induced gene expression cascade via binding to
the promoters of their respective cis-acting elements, majorly dehydration-responsive ele-
ment (DRE) or C-repeat (CRT), abscisic acid response element (ABRE), and myelocytoma-
tosis regulatory similarities (MYCRS)/ myeloblastosis regulatory similarities (MYBRS),
respectively (Bhattacharjee and Jain 2013; Roychoudhury and Sengupta 2009). Selected
reports also emphasize that both ABA-dependent and ABA-independent pathways are
exclusively associated only under cold acclimation, thereby excluding salinity and drought
stresses (Mauch-Mani and Mauch 2005). ABA levels are said to vary constantly depending
upon the external responses where a low ABA level helps to release the seed dormancy
during seed germination. By contrast, a high level of this hormone is maintained mostly
under abiotic stress, thereby arresting the growth until the normal conditions are resumed
(Roychoudhury et al. 2009a,b). Viewing holistically, stress tolerance in plants is a complex
term as they usually perceive multiple stresses simultaneously during their course of devel-
opment. Stress typically leads to cell desiccation further leading to membrane damage and
thereby results in osmotic imbalance. Osmotic imbalance and membrane damage are the
final consequences of extreme cell injury, which are reported to enhance the expression
level of stress-related genes and their corresponding downstream transcription factors
(Roychoudhury et al. 2008b). This was a common phenomenon visualized after cold,
drought, high salinity, or separately after applying exogenous ABA (Tuteja 2007). Calcium
has proven role as a secondary messenger against multiple environmental stresses; there-
fore, calcium-mediated signal transduction signifies to be a strong candidate that might be
8. 11.3 Role of Specialized Stress-responsive Hormone 261
involved in mediating these intermediate signals. Studies have established a relation
between augmented levels of calcium, which results from ABA, drought, cold, and high
salt treatment in plants (Tuteja 2007). Further studies demonstrated the role of several
known stress markers as well as key transcription factors to be upregulated under stress
and by ABA application in a similar fashion. The transcript levels of a drought-responsive
(RD29A) gene were found to be regulated in ABA-dependent as well as in ABA-independent
manners (Basu and Roychoudhury 2014a,b). Similarly, another type of stress marker,
namely proline, is accumulated in plants facing stress, and was also known to be influ-
enced both by ABA-dependent and ABA-independent signaling pathways (Mahajan and
Tuteja 2005). Considering the abovementioned reports, it can be concluded that numerous
stress signals in coordination with stress hormone ABA stake several overlapping compo-
nents of signaling pathways highly interrelated with each other, to maintain cellular
homeostasis.
11.3.2 Brassinosteroids
BRs fall under naturally occurring steroidal group of polyhydroxylated plant hormones
having a major function in growth and developmental process namely regulating processes
that include cellular expansion and proliferation, male fertility, vascular differentiation,
senescence, and development of leaves (Banerjee and Roychoudhury 2018a). Apart from
the abovementioned roles, these steroidal derivatives also function as major players for
stress mitigation and regulation. BRs regulate plant growth and stress responses via inter-
acting with downstream transcription factors via a series of signaling cascades, governing
a number of downstream genes. BRs also interact with several plant growth hormones
resulting in enhanced tolerance against several abiotic stresses, namely heat, cold, drought,
salinity, and biotic stresses triggered by bacterial and fungal pathogens. Reports suggest
that BR application alters both enzymatic and nonenzymatic antioxidants (Fariduddin
et al. 2014). Studies emphasize that brassinolide (BL, a BR derivative) treatment in stress-
imposed maize seedlings results in increased activities of enzymes such as superoxide dis-
mutase (SOD), ascorbate peroxidase, catalase (CAT), and antioxidants such as carotenoid
and ascorbic acid (Li et al. 1998). BRs were also reported to enhance the activity of CAT in
sorghum plants imposed with osmotic stress (Vardhini and Rao 2003). Rice seedlings sub-
jected to salinity stress when treated with BRs showed a significant enhancement in activi-
ties of CAT, SOD, and glutathione reductase (GR) (Nunez et al. 2003). Studies signify the
prominent role of BRs in regulating stress tolerance via modulating the ROS generation
and scavenging cascades, thus assisting plants toward stress adaptations (Fariduddin et al.
2014). Apart from imparting tolerance under abiotic stress, brassinosteroids are known to
work efficiently under biotic stress, as per the reports. Fourteen-day-old tomato seedlings
in presence of exogenously applied 24-epibrassinolide (EBR) were able to minimize the
disease symptoms caused by Verticillium dahliae. EBR-treated tomato plants did not show
any or very low disease symptoms, whereas moderate to severe symptoms were recorded in
majority of untreated plants. Treatment with similar brassinosteroid derivative, BL, was
able to provoke resistance against infection of tobacco mosaic virus in tobacco plants as
well as against Magnaporthe grisea and Xanthomonas oryzae in rice plants, known patho-
gens causing rice blast and bacterial blight, respectively (Nakashita et al. 2003). A similar
9. 11 Role of Growth Regulators and Phytohormones in Overcoming Environmental Stress
262
study reports an elevated H2O2 level in BR-treated plants, resulting from imbalanced ROS,
further justifying ROS to be the primary defense signal for a better protection under oxida-
tive stress. In addition, reports also indicate that an augmented accumulation of ROS and
enhanced calcium influx is able to trigger the activation of mitogen-activated protein
kinase (MAPK), where MAPK cascades play a pivotal role in plant defense against patho-
gen attack (Xia et al. 2009). Thus, ROS and MAPKs may overall assist in developing a posi-
tive feedback loop for rapid signal transmission, an utmost requirement for systemic
signaling for regulating plant responses toward multiple environmental vagaries
(Xia et al. 2009).
11.3.3 Jasmonic Acid
Plants produce a diversity of compounds from flowers, fruits, and several other vegetative
tissues that are mostly volatile. These compounds attract specific pollinators or may assist
them to communicate with their surroundings, therefore preparing them to counter the
deleterious effects of harmful insects (Sembdner and Parthier 1993; Pichersky and
Gershenzon 2002). Among them, jasmonic acid is a naturally occurring plant growth regu-
lator found in higher plants. Roots and leaves are the major sites for inhibition via jasmonic
acid where chloroplasts and peroxisomes are major sites for JA biosynthesis (Cheong and
Do Choi 2003). A scented volatile compound termed as methyl jasmonate (MeJA), isolated
from Jasminum grandiflorum flowers, is distributed universally in plants. Methyl jas-
monate and jasmonic acid (free acid of methyl jasmonate) both are collectively termed as
jasmonates, and are cellular regulators having proven roles in activating plant defense
mechanisms under stress conditions. In addition, jasmonates also trigger plant defense
mechanisms during insect attack, mechanical wounding, pathogenic stresses, and environ-
mental stress, namely drought, salinity, and temperature (Wasternack and Parthier 1997;
Paré and Tumlinson 1999). In addition to their property of stress induction, these com-
pounds being volatile also act as airborne signals targeting not only the infected crop but
also its surrounding crops (Arimura et al. 2000). MeJA treatment is known to upregulate
genes related to biosynthesis of jasmonate, secondary metabolites, formation of cell wall,
and genes encoding proteins for stress acclimation. On the contrary, the photosynthesis-
related genes mainly are the genes encoding ribulose bisphosphate carboxylase/oxygenase,
genes coding for light-harvesting complex II, and chlorophyll a-/chlorophyll b-binding
protein-related genes that are downregulated by MeJA treatment further justifying their
role in temporarily ceasing plant growth for countering stress in a better manner (Cheong
and Do Choi 2003). Recent reports indicated a differential enhancement in JA levels in two
different tomato cultivars where an elevated level of JA was observed in tolerant cultivar,
while a reduced level was recorded in salt-sensitive cultivar post 24hours salt treatment
(Pedranzani et al. 2003). Similar reports substantiating the role of MeJA under stress were
demonstrated by Moons et al. (1997), where 200mM NaCl was able to significantly enhance
the JA levels in roots of rice plant. Additionally, another study concludes that drought
stress stimulates the expression of similar set of transcripts that are regulated via jasmonic
acid (Mason and Mullet 1990; Bell and Mullet 1991). Similar reports emphasize that very
low concentrations of jasmonates were found to regulate biotic stress-responsive genes,
encoding proteinase inhibitors and enzymes involved in flavonoid biosynthesis, namely
10. 11.3 Role of Specialized Stress-responsive Hormone 263
chalcone synthase and phenylalanine ammonia lyase (Farmer and Ryan 1990). Jasmonates
were also shown to induce expression of lipoxygenase enzyme that holds a key role in
pathogenesis (Creelman et al. 1992). Apart from their protective roles, jasmonates are also
reported to induce senescence at high exogenous concentrations; however a question still
prevails whether this is capable of modulating senescence in vitro. The cross talk of JA with
other hormones was substantiated by an experiment where applying JA exogenously
altered the endogenous level of abscisic acid, a major stress-responsive hormone. This
JA-mediated regulation in ABA level was recognized as an important link for delineating
the protective role against salt stress (Kang et al. 2005). Therefore, it can be concluded that
tolerant plants exhibiting an augmented level of JA under salt stress may indicate an effec-
tive protection strategy against stress.
11.3.4 Salicylic Acid
Salicylic acid or orthohydroxy benzoic is another well-recognized growth hormone that is
identified to impart disease resistance and combating stress in plants. Other roles of this
hormone are regulating germination of seeds, regulating flowering and fruit yield, and ion
transport (Klessig and Malamy 1994; Harper and Balke 1981; Khan et al. 2003). Reports
indicated the function of this hormone in abating the oxidative stress-induced damage via
modulating antioxidant defense in plants (Shirasu et al. 1997). It is accepted to be a signal-
controlling response to several abiotic stresses, namely water deficit (Munne-Bosch and
Penuelas 2003; Chini et al. 2004), cold and chilling (Janda et al. 1999; Kang and Saltveit
2002), tolerance against heavy metals (Metwally et al. 2003; Yang et al. 2003; Freeman et al.
2005), high temperature (Larkindale and Knight 2002; Larkindale et al. 2005), and osmotic
imbalance (Borsani et al. 2001). This abatement is mediated by regulating pathways for
photosynthesis, nitrogen metabolism, and osmolyte metabolism, such as proline and gly-
cine betaine metabolism (Nazar et al. 2011; Miura and Tada 2014), and genes that code for
heat shock proteins (HSPs), enzymatic and nonenzymatic antioxidants, and various types
of secondary metabolites. Moreover, the role is not confined to abiotic stress amelioration
but also to protect plants against biotic stress mediated via MAPK pathway. SA also induces
oxidative burst, which results in apoptotic and hypersensitive response, further transduc-
ing the signal downstream for triggering systemic acquired resistance (Shirasu et al. 1997).
In addition, SA is known to interact with other signaling molecules (NO and H2O2); how-
ever, very few studies listed in the following text support this rational. SA was reported to
augment H2O2 levels by inhibiting catalase and thus playing a pivotal part in regulating the
initiation of toxic molecules, namely ROS (Horváth et al. 2002). Moderate dose of SA when
applied exogenously increased the abiotic stress resistance in plants (Senaratna et al. 2000;
Tari et al. 2002). Pretreatment of maize plants with SA was shown to stimulate ROS-
mediated alterations in the activities of several enzymes of antioxidant pathway, subse-
quently increasing the chilling tolerance (Janda et al. 1999). In a similar study, mustard
seedlings when treated with exogenous SA displayed a better thermotolerance and
enhanced heat acclimation (Dat et al. 2000b). This could be utilized as a potential strategy
for plant protection to environmental vagaries, as moderate dose of SA can influence H2O2-
mediated alteration in ROS levels, thus activating the overall antioxidative defense mecha-
nism in plants (Roychoudhury et al. 2016).
11. 11 Role of Growth Regulators and Phytohormones in Overcoming Environmental Stress
264
11.3.5 Strigolactones
SL is a unique member of phytohormone family known to be recently characterized. Till
now, 17 SLs have been isolated from diverse crop species and are known to be synthesized
in the roots and released in rhizosphere. SLs were earlier known to act as a stimulant for
host-derived germination enhancement. Strigolactones are reported to inhibit bud
growth (Gomez-Roldan et al. 2008; Umehara et al. 2008), in contrast cytokinins promote
growth of buds (Wickson and Thimann 1958), thus complimenting the downward move-
ment of auxins in the vascular cambium cells, where auxins are mostly unable to move
upward into buds. Therefore, cytokinins and strigolactones work in contrast as secondary
messengers for bud arrest (Brewer et al. 2009; Dun et al. 2009) and conversely both are
known to be negatively regulated by auxin (Dun et al. 2009; Banerjee and
Roychoudhury 2018b).
A recent research has emphasized their vital role as being a signal for detection of host
and branching of hyphae during infection of arbuscular mycorrhizal fungi (AMF)
(Akiyama et al. 2005; Besserer et al. 2006). Thus, they help the AMF to contact the hosts
and colonize them into the roots by inducing hyphal branching. Conclusive evidences
through supportive literature have included them in the phytohormone family for having
an additional role of regulating root and shoot architecture along with their indigenous
role as being a signal for host detection (Gomez-Roldan et al. 2008; Umehara et al. 2008).
Majority of studies emphasize their role in plant interaction with root symbionts and
weeds where an increased concentration of strigolactones around the root zone increases
the infection of AMF, which in turn helps the plant to uptake increased nutrient and
water from the soil during nutrient scarcity (Ruyter-Spira et al. 2013; Waldie et al. 2014;
Al-Babili and Bouwmeester 2015; Zhang et al. 2015). It is reported that under suboptimal
nutrient availability such as phosphate deprivation, levels of strigolactone are known to
increase in order to optimize plant’s growth to suit the external adverse environment
(Umehara et al. 2008; Kohlen et al. 2011). In a study conducted by Yoneyama et al. 2007,
levels of strigolactone were reported to augment the growth of red clover under phos-
phate-deprived conditions. It was concluded that increased hyphal branching of arbus-
cular mycorrhizal fungi was a result of strigolactones that were extracted from plant
roots (Akiyama et al. 2005). It is now a typical practice in agriculture to impose phos-
phate deprivation to enhance the exceedingly abundant strigolactones in plants
(Yoneyama et al. 2007). Other recent studies strongly emphasizing their connection in
mitigating abiotic stress also came into the picture (Saeed et al. 2017, Pandey et al. 2016).
In addition, their function is also evident in seed germination, stress mitigation, and
defining the plant architecture. Reports indicated that a hypersensitive response in SLs
depleted plants of A. thaliana and Lotus japonicus (Liu et al. 2015) against water deficit
stress in shoots. Studies indicate a possible interaction of SLs with two key hormones,
particularly auxins and ABA. Cheng et al. (2013) inferred a key role of SLs in plant
growth and development during suboptimal environmental conditions. Similar results
were observed in both the crops for stomata that become hypersensitive toward endoge-
nous and exogenous ABA. All these findings led to the possibility toward the function of
strigolactone in environmental stress mitigation in the plants (Van Ha et al. 2014; Liu
et al. 2015) (Figure 11.1).
12. 11.4 Hormone Cross Talk and Stress Alleviatio 265
11.4
Hormone Cross Talk and Stress Alleviation
There is a strong relationship between hormone signaling and plant defense against various
environmental stresses. Plants need to carefully utilize their water and food resources under
stressful conditions, which sometimes require a transient inhibition of growth and develop-
ment, as provided by some growth regulators, and in turn plants get ready to tolerate the
adverse implications of stress. As primarily these phytohormones are involved in regulating
plant growth and overall development, they are assigned as the first target to be regulated
in order to balance the resource utilization and hence a strong cross talk between hormone
ABIOTIC STRESS BIOTIC STRESS
Signal Perception &
hormone signaling
Aux/CK
NAC (RD26), MYB, MYC,
AREB/ABF(bZIP), WRKY
Transcription factor
NAC, DREB2/AP2,
DREB1/CBF Transcription
factors
Stress
Response
BR, SL’s, GA, MeJA
ROS
ABA Dependent
Cross talk/
Signaling
ABA
Independent
Pathway
cis cis
Figure 11.1 A schematic diagram depicting phytohormone-mediated stress alleviation: A complex
interplay of signaling components in plants.
13. 11 Role of Growth Regulators and Phytohormones in Overcoming Environmental Stress
266
signaling and its downstream genes is required for maintaining internal homeostasis under
stressful conditions. The growth regulators, namely auxins, cytokinins, and gibberellins,
are major key players maintaining growth during stressful regimes (Peleg and Blumwald
2011). During suboptimal conditions, stress hormone ABA and gaseous hormone ethylene
inhibit growth by modulating actions of other hormones, namely auxins, cytokinins, and
GA (Achard et al. 2006; Wolters and Jürgens 2009; Peleg and Blumwald 2011). Several case
studies indicating the effects of various phytohormones interacting together, either syner-
gistically or antagonistically, leading to stress tolerance are listed in the following text.
11.4.1 ABA-mediated Signaling with Auxin and Cytokinin
Indole-3-acetic acid is an auxin recognized to counter deleterious effects of drought and
provide tolerance. Additionally, it is also reported to enhance the expression of LEA (late
embryogenesis abundant) genes providing enhanced tolerance against drought in seed-
lings of rice (Zhang et al. 2009b). Conversely, auxin also regulated a key intermediate of
ethylene biosynthesis, 1-amino-cyclopropane-1-carboxylate synthase (ACS) gene, where
auxin treatment was shown to encode rate-limiting enzymes in ethylene biosynthesis
(Tsuchisaka and Theologis 2004). At molecular level, auxins are potentially involved in
regulating the level of ABI5-Like1 (ABL1), a bZIP transcriptional factor in rice, known to
be primarily stimulated by drought, salinity, and osmotic stresses. The bZIP transcriptional
factor is known to transcriptionally activate numerous downstream genes that are majorly
stress responsive, which include common ABRE elements containing WRKY and genes
corresponding to auxin metabolism, via binding with respective elements (Yang et al. 2011;
Banerjee and Roychoudhury 2015). Apart from auxin, another growth hormone cytokinin
is reported to be regulated by ABA via feedback regulatory loop and was shown to be
involved in downstream signaling for maintaining appropriate levels of both these hor-
mones (Jones et al. 2010). In addition, the expression of isopentenyl transferase (IPT), a
gene encoding a key step in the biosynthesis of cytokinin, is regulated via stress-inducible
promoter in tobacco. This significant alteration in gene expression under stress was found
to be coupled with response, regulation, and biosynthesis of phytohormones (Peleg et al.
2011). Exogenous application of ABA was reported to downregulate IPT gene as revealed
by gene expression studies; however, augmented levels of some gene products were
recorded for cytokinin oxidases and dehydrogenases highlighting its implied role during
stress (Nishiyama et al. 2011). In another study, increased level of cytokinin in transgenic
tomato roots over expressing IPT gene was reported to alter the level growth hormones
under saline conditions (Ghanem et al. 2010). This was further corroborated in studies con-
ducted using rice plants where accumulation in cytokinin level resulted in a stay-green
type of phenotype with better yield under water-deficit stress, obtained by using a tissue-
specific promoter (Peleg et al. 2011). During stressful conditions, ABA is also known to
respond to ethylene, brassinosteroid, jasmonic acid, and salicylic acid, and has a prominent
role in regulating stomatal opening (Acharya and Assmann 2009). Abscisic acid, brassinos-
teroid, jasmonic acid, salicylic acid, and nitric acid induce stomatal closure, whereas
cytokinins and auxins promote stomatal opening, thus highlighting their prominence in
regulating water homeostasis. A negative correlation exists among ABA and other
hormones, as under stressful conditions levels of cytokinins were found to decline with a
14. 11.4 Hormone Cross Talk and Stress Alleviatio 267
concomitant increase in ABA levels (Pospisilova et al. 2005). This complex interplay of
ABA with other hormones was found crucial for stress signaling.
11.4.2 ABA-mediated Signaling with GA and MeJA
An association of gibberellins in stress mitigation is evident elucidating after several reports
indicated that DELLA proteins, known transcriptional repressor of GA, are involved in its
subsequent degradation through 26S proteasomal pathway. GA and other related proteins
are central modulators of plant development under various environmental stresses. GID1
was reported as the receptor for plant hormone gibberellic acid for regulating downstream
genes responsible for GA production (Fleet and Sun 2005). Modes of action of ABA and
ethylene are antagonistic to the action of GA; this cross talk is mediated mainly at the level
of DELLA protein (Achard et al. 2006; Wolters and Jürgens 2009). Apart from this, DELLA
is also known to coordinate homeostasis of GA and establish a link between GA and ABA
(Hirano et al. 2008; Stamm and Kumar 2010; Stamm et al. 2012). Additionally, GA is also
known to interact with brassinosteroid and salicylic acid for eliciting numerous physiologi-
cal processes (Beaudoin et al. 2000; Xu et al. 2006). Similarly, ABA was found to be associ-
ated with JA in experiments performed by Kim et al. (2009) where levels of both methyl
jasmonate and abscisic acid were found elevated under drought stress, which resulted in a
declined seed set in rice panicles. The similar decline in seed set was also obtained when
MeJA gene was overexpressed in transgenic rice; the resulting lines exhibited a poor grain
yield with a concomitant increase in ABA levels. ABA is also known to stimulate MeJA-
induced stomatal closure in A. thaliana (Hossain et al. 2011). In addition, Lackman et al.
(2011) identified an association between the ABA receptor and JA responses in hormoniz-
ing growth and stress adaptation. All the abovementioned reports further strengthen the
notion that a cross talk must exist between biosynthesis of MeJA and ABA and several
other phytohormones to regulate further stress signaling.
11.4.3 ABA-mediated Signaling with Strigolactone
As strigolactone and ABA both possess the same precursor pool of carotenoids, strigolac-
tone biosynthesis is also known to be regulated by carotenoid cleavage (cc) dioxygenase
genes, namely CCD7 and CCD8. This common precursor had led the hypothesis that ABA
and strigolactone biosynthesis processes may be interdependent and interconnected
somehow. It is now reported and validated that biosynthesis of strigolactone in plants is
induced by ABA (Lopez-Raez et al. 2010). Recently, the role of strigolactone through
orchestrating auxin and ethylene levels, for root growth and regulation, has been reported
(Koltai 2011). Root development being an important parameter induced under drought
and starvation for increased water and mineral absorption further corroborates its vital
role for tolerance toward abiotic stresses. This also helps in formulating a hypothesis that
during suboptimal conditions plants often commit an untimely response toward stress
and decline the growth and development via inhibiting nutrient acquisition, thus ceasing
the growth temporarily until the stress vanishes (Skirycz et al. 2011a). Hence, it is clear
that these specialized hormones display a complex cross talk and play a central role in
stress mitigation in plants.
15. 11 Role of Growth Regulators and Phytohormones in Overcoming Environmental Stress
268
11.4.4 ABA-mediated Signaling with Brassinosteroids
Brassinosteroids when applied exogenously are reported to significantly enhance the ABA
levels under stress (Liu et al. 2009; Zhang et al. 2011). However, various reports have catego-
rized ABA and JA to be antagonistic for eliciting various biological and physiological responses
such as seed germination, closure of stomata, root growth, and premature seedling develop-
ment in plants (Steber and McCourt 2001; Zhang et al. 2009a). A recent study supports
BR-mediated inhibition of ABA signaling where the root length and seed germination in BR
mutants bri1, bin2-1, and det2-1 were found more affected with ABA, in comparison to wild-
type plants (Choe et al. 2002; Clouse et al. 1996; Li et al. 2001; Steber and McCourt 2001; Xue
et al. 2009). A similar study performed on Arabidopsis also highlighted that a substantial
enhancement was recorded in mutant plants found defective in ABA biosynthesis (Divi et al.
2010). Various components of ROS and nitric oxide signaling were found to play a common
association between ABA-mediated and BR-mediated stress tolerance (Xia et al. 2009, 2011).
A study highlighted that BR-induced generation of ROS was a prerequisite in BR-mediated
stress tolerance in plants of cucumber and tomato (Xia et al. 2009). Several studies have
depicted the role of exogenous BRs in significantly augmenting the ABA accumulation under
stress conditions (Kurepin et al. 2008; Liu et al. 2009; Zhang et al. 2011). BR was also shown to
trigger a transient enhancement in expression of respiratory burst oxidase homolog 1 (RBOH1)
transcript, activity of nicotinamide adenine dinucleotide phosphate (NADPH) oxidase, and
H2O2 and nitric oxide (NO) levels in apoplast (Cui et al. 2011; Nie et al. 2013). Similarly reports
conclude that ABA induces the activities of NADPH oxidase and RBOH transcripts, thus regu-
lating H2O2 accumulation in apoplasts justifying a strong interconnection between ABA-
mediated and BR-mediated stress signaling (Pei et al. 2000; Kwak et al. 2003).
11.5
Conclusions and Future Perspective
Phytohormones play an important role in regulating plant growth and development as well
as in alleviation of several stressful conditions. Among phytohormones, abscisic acid plays
a crucial role in mediating cross talk with other phytohormones and further activating the
downstream components of the signaling pathway in response to stress. Notably, phytohor-
mones can act in synergetic or antagonistic manner to overcome stress. However, a com-
plex interplay between the phytohormones and other key stress-responsive players acts as
an adaptive response under stress conditions. Taking a cue from the compiled information,
it can be suggested that a common mechanism of action exists for different types of stresses,
and phytohormones mediate the regulation of various genes and transcription factors asso-
ciated with antioxidant pathways and other stress-related genes in a coordinated fashion to
cope up with the deleterious effects of stressful environment.
References
Abdullah, Z. and Ahmad, R. (1990). Effect of pre-and post-kinetin treatments on salt tolerance
of different potato cultivars growing on saline soils. Journal of Agronomy and Crop Science
165 (2-3): 94–102.
16. Reference 269
Abeles, F.W. (1992). Roles and physiological effects of ethylene in plant physiology: dormancy,
growth, and development. In: Ethylene in Plant Biology (eds. F.B. Abeles, P.W. Morgan and
M.E. Saltveit Jr.), 120–181. Academic Press, INC.
Achard, P., Cheng, H., De Grauwe, L. et al. (2006). Integration of plant responses to
environmentally activated phytohormonal signals. Science 311 (5757): 91–94.
Achard, P., Gong, F., Cheminant, S. et al. (2008). The cold-inducible CBF1 factor–dependent
signaling pathway modulates the accumulation of the growth-repressing DELLA proteins
via its effect on gibberellin metabolism. The Plant Cell 20 (8): 2117–2129.
Acharya, B.R. and Assmann, S.M. (2009). Hormone interactions in stomatal function. Plant
Molecular Biology 69 (4): 451–462.
Afzal, I., Basra, S.A., and Iqbal, A. (2005). The effects of seed soaking with plant growth
regulators on seedling vigor of wheat under salinity stress. Journal of Stress Physiology &
Biochemistry 1 (1).
Akbari, G., Sanavy, S.A., and Yousefzadeh, S. (2007). Effect of auxin and salt stress (NaCl) on
seed germination of wheat cultivars (Triticum aestivum L.). Pakistan Journal of Biological
Sciences 10 (15): 2557–2561.
Akiyama, K., Matsuzaki, K.I., and Hayashi, H. (2005). Plant sesquiterpenes induce hyphal
branching in arbuscular mycorrhizal fungi. Nature 435 (7043): 824.
Al-Babili, S. and Bouwmeester, H.J. (2015). Strigolactones, a novel carotenoid-derived plant
hormone. Annual Review of Plant Biology 66: 161–186.
Apel, K. and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress, and signal
transduction. Annual Review of Plant Biology 55: 373–399.
Arimura, G.I., Ozawa, R., Shimoda, T. et al. (2000). Herbivory-induced volatiles elicit defence
genes in lima bean leaves. Nature 406 (6795): 512.
Banerjee, A. and Roychoudhury, A. (2015). WRKY proteins: signaling and regulation of
expression during abiotic stress responses. The Scientific World Journal 2015: 807560.
Banerjee, A. and Roychoudhury, A. (2018a). Interactions of brassinosteroids with major
phytohormones: antagonistic effects. Journal of Plant Growth Regulation 37: 1025–1032.
Banerjee, A. and Roychoudhury, A. (2018b). Strigolactones: multi-level regulation of
biosynthesis and diverse responses in plant abiotic stresses. Acta Physiologiae Plantarum
40: 86.
Banerjee, A. and Roychoudhury, A. (2019). The regulatory signaling of gibberellin metabolism
and its crosstalk with phytohormones in response to plant abiotic stresses. In: Plant
Signaling Molecules (eds. M.I.R. Khan, P.S. Reddy, A. Ferrante and N.A. Khan), 333–339.
United Kingdom: Woodhead Publishing (Elsevier).
Barciszewski, J., Siboska, G., Rattan, S.I., and Clark, B.F. (2000). Occurrence, biosynthesis and
properties of kinetin (N6-furfuryladenine). Plant Growth Regulation 32 (2–3): 257–265.
Basalah, M.O. and Mohammad, S. (1999). Effect of salinity and plant growth regulators on
seed germination of Medicago sativa L. Pakistan Journal of Biological Sciences 2: 651–653.
Basu, S. and Roychoudhury, A. (2014a). Expression profiling of abiotic stress-inducible genes
in response to multiple stresses in rice (Oryza sativa L.) varieties with contrasting level of
stress tolerance. BioMed Research International 2014: 706890.
Basu, S. and Roychoudhury, A. (2014b). Inducibility of dehydration responsive element
(DRE)-based promoter through gusA expression in transgenic tobacco. Indian Journal of
Biotechnology 13: 172–177.
17. 11 Role of Growth Regulators and Phytohormones in Overcoming Environmental Stress
270
Beaudoin, N., Serizet, C., Gosti, F., and Giraudat, J. (2000). Interactions between abscisic acid
and ethylene signaling cascades. The Plant Cell 12 (7): 1103–1115.
Bell, E. and Mullet, J.E. (1991). Lipoxygenase gene expression is modulated in plants by water
deficit, wounding, and methyl jasmonate. Molecular and General Genetics MGG 230 (3):
456–462.
Berleth, T., Krogan, N.T., and Scarpella, E. (2004). Auxin signals—turning genes on and
turning cells around. Current Opinion in Plant Biology 7 (5): 553–563.
Besserer, A., Puech-Pagès, V., Kiefer, P. et al. (2006). Strigolactones stimulate arbuscular
mycorrhizal fungi by activating mitochondria. PLoS Biology 4 (7): e226.
Bhattacharjee, A. and Jain, M. (2013). Transcription factor mediated abiotic stress signaling in
rice. Plant Stress 7: 16–25.
Borsani, O., Valpuesta, V., and Botella, M.A. (2001). Evidence for a role of salicylic acid in the
oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant
Physiology 126 (3): 1024–1030.
Boucaud, J. and Ungar, I.A. (1976). Hormonal control of germination under saline conditions
of three halophytic taxa in the genus Suaeda. Physiologia Plantarum 37 (2): 143–148.
Boylan, M.T. and Quail, P.H. (1989). Oat phytochrome is biologically active in transgenic
tomatoes. The Plant Cell 1 (8): 765–773.
Bozcuk, S. (1981). Effects of kinetin and salinity on germination of tomato, barley and cotton
seeds. Annals of Botany 48 (1): 81–84.
Brewer, P.B., Dun, E.A., Ferguson, B.J. et al. (2009). Strigolactone acts downstream of auxin to
regulate bud outgrowth in pea and Arabidopsis. Plant Physiology 150 (1): 482–493.
Chakrabarti, N. and Mukherji, S. (2003). Alleviation of NaCl stress by pretreatment with
phytohormones in Vigna radiata. Biologia Plantarum 46 (4): 589–594.
Chang-cheng, X. and Qi, Z. (1993). Effect of drought on lipoxygenase activity, ethylene and
ethane production in leaves of soybean plants. Acta Botanica Sinica (China): –31, 37.
Cheng, X., Ruyter-Spira, C., and Bouwmeester, H. (2013). The interaction between
strigolactones and other plant hormones in the regulation of plant development. Frontiers
in Plant Science 4: 199.
Cheong, J.J. and Do Choi, Y. (2003). Methyl jasmonate as a vital substance in plants. Trends in
Genetics 19 (7): 409–413.
Cheong, Y.H., Chang, H.S., Gupta, R. et al. (2002). Transcriptional profiling reveals novel
interactions between wounding, pathogen, abiotic stress, and hormonal responses in
Arabidopsis. Plant Physiology 129 (2): 661–677.
Chini, A., Grant, J.J., Seki, M. et al. (2004). Drought tolerance established by enhanced
expression of the CC–NBS–LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1.
The Plant Journal 38 (5): 810–822.
Choe, S., Schmitz, R.J., Fujioka, S. et al. (2002). Arabidopsis Brassinosteroid-insensitive
dwarf12 mutants are semidominant and defective in a glycogen synthase kinase 3β-like
kinase. Plant Physiology 130 (3): 1506–1515.
Clouse, S.D., Langford, M., and McMorris, T.C. (1996). A brassinosteroid-insensitive mutant in
Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiology
111 (3): 671–678.
Colebrook, E.H., Thomas, S.G., Phillips, A.L., and Hedden, P. (2014). The role of gibberellin
signalling in plant responses to abiotic stress. Journal of Experimental Biology 217 (1): 67–75.
18. Reference 271
Creelman, R.A., Tierney, M.L., and Mullet, J.E. (1992). Jasmonic acid/methyl jasmonate
accumulate in wounded soybean hypocotyls and modulate wound gene expression.
Proceedings of the National Academy of Sciences of the United States of America 89 (11):
4938–4941.
Cui, J.X., Zhou, Y.H., Ding, J.G. et al. (2011). Role of nitric oxide in hydrogen peroxide-
dependent induction of abiotic stress tolerance by brassinosteroids in cucumber. Plant, Cell
& Environment 34 (2): 347–358.
Dat, J.F., Lopez-Delgado, H., Foyer, C.H., and Scott, I.M. (2000b). Effects of salicylic acid on
oxidative stress and thermotolerance in tobacco. Journal of Plant Physiology 156 (5-6):
659–665.
Davies, P.J. (2004). Plant Hormones: Biosynthesis, Signal Transduction, Action. Publisher
Springer.
Davletova, S., Rizhsky, L., Liang, H. et al. (2005). Cytosolic ascorbate peroxidase 1 is a central
component of the reactive oxygen gene network of Arabidopsis. The Plant Cell 17 (1):
268–281.
De Lucas, M., Daviere, J.M., Rodríguez-Falcón, M. et al. (2008). A molecular framework for
light and gibberellin control of cell elongation. Nature 451 (7177): 480.
Divi, U.K., Rahman, T., and Krishna, P. (2010). Brassinosteroid-mediated stress tolerance in
Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways.
BMC Plant Biology 10 (1): 151.
Dun, E.A., Brewer, P.B., and Beveridge, C.A. (2009). Strigolactones: discovery of the elusive
shoot branching hormone. Trends in Plant Science 14 (7): 364–372.
Dunlap, J.R. and Binzel, M.L. (1996). NaCI reduces indole-3-acetic acid levels in the roots of
tomato plants independent of stress-induced abscisic acid. Plant Physiology 112 (1):
379–384.
Fariduddin, Q., Yusuf, M., Ahmad, I., and Ahmad, A. (2014). Brassinosteroids and their role in
response of plants to abiotic stresses. Biologia Plantarum 58 (1): 9–17.
Farmer, E.E. and Ryan, C.A. (1990). Interplant communication: airborne methyl jasmonate
induces synthesis of proteinase inhibitors in plant leaves. Proceedings of the National
Academy of Sciences of the United States of America 87 (19): 7713–7716.
Feng, S., Martinez, C., Gusmaroli, G. et al. (2008). Coordinated regulation of Arabidopsis
thaliana development by light and gibberellins. Nature 451 (7177): 475.
Fleet, C.M. and Sun, T.P. (2005). A DELLAcate balance: the role of gibberellin in plant
morphogenesis. Current Opinion in Plant Biology 8 (1): 77–85.
Freeman, J.L., Garcia, D., Kim, D. et al. (2005). Constitutively elevated salicylic acid signals
glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant
Physiology 137 (3): 1082–1091.
Ghanem, M.E., Albacete, A., Smigocki, A.C. et al. (2010). Root-synthesized cytokinins improve
shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.) plants. Journal
of Experimental Botany 62 (1): 125–140.
Gomez-Roldan, V., Fermas, S., Brewer, P.B. et al. (2008). Strigolactone inhibition of shoot
branching. Nature 455 (7210): 189.
GroBelindemann, E., Graebe, J.E., Stockl, D., and Hedden, P. (1991). Ent-Kaurene biosynthesis
in germinating barley (Hordeum vulgare L., cv Himalaya) caryopses and its relation to
a-amylase production. Plant Physiology 96: 1099–1104.
19. 11 Role of Growth Regulators and Phytohormones in Overcoming Environmental Stress
272
Guilfoyle, T.J., Hagen, G., Li, Y. et al. (1993). Auxin-regulated transcription. Functional Plant
Biology 20 (5): 489–502.
Hagen, G. and Guilfoyle, T. (2002). Auxin-responsive gene expression: genes, promoters and
regulatory factors. Plant Molecular Biology 49 (3-4): 373–385.
Harper, J.R. and Balke, N.E. (1981). Characterization of the inhibition of K+ absorption in oat
roots by salicylic acid. Plant Physiology 68 (6): 1349–1353.
Hirano, K., Ueguchi-Tanaka, M., and Matsuoka, M. (2008). GID1-mediated gibberellin
signaling in plants. Trends in Plant Science 13 (4): 192–199.
Hisamatsu, T., Koshioka, M., Kubota, S. et al. (2000). The role of gibberellin biosynthesis in the
control of growth and flowering in Matthiola incana. Physiologia Plantarum 109 (1): 97–105.
Horváth, E., Janda, T., Szalai, G., and Páldi, E. (2002). In vitro salicylic acid inhibition of
catalase activity in maize: differences between the isozymes and a possible role in the
induction of chilling tolerance. Plant Science 163 (6): 1129–1135.
Hossain, M.A., Munemasa, S., Uraji, M. et al. (2011). Involvement of endogenous abscisic acid
in methyl jasmonate-induced stomatal closure in Arabidopsis. Plant Physiology https://doi.
org/10.1104/pp.111.172254.
Hyodo, H., Tanaka, K., and Suzuki, T. (1991). Wound-induced ethylene synthesis and its
involvement in enzyme induction in mesocarp tissue of Cucurbita maxima. Postharvest
Biology and Technology 1 (2): 127–136.
Iqbal, M. and Ashraf, M. (2013). Gibberellic acid mediated induction of salt tolerance in wheat
plants: growth, ionic partitioning, photosynthesis, yield and hormonal homeostasis.
Environmental and Experimental Botany 86: 76–85.
Iqbal, M., Ashraf, M., and Jamil, A. (2006). Seed enhancement with cytokinins: changes in
growth and grain yield in salt stressed wheat plants. Plant Growth Regulation 50 (1): 29–39.
Janda, T., Szalai, G., Tari, I., and Paldi, E. (1999). Hydroponic treatment with salicylic acid
decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208 (2):
175–180.
Jones, B., Gunnerås, S.A., Petersson, S.V. et al. (2010). Cytokinin regulation of auxin synthesis
in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin
signal transduction. The Plant Cell https://doi.org/10.1105/tpc.110.074856.
Jordan, E.T., Hatfield, P.M., Hondred, D. et al. (1995). Phytochrome A overexpression in
transgenic tobacco (correlation of dwarf phenotype with high concentrations of phytochrome
in vascular tissue and attenuated gibberellin levels). Plant Physiology 107 (3): 797–805.
Kang, H.M. and Saltveit, M.E. (2002). Chilling tolerance of maize, cucumber and rice seedling
leaves and roots are differentially affected by salicylic acid. Physiologia Plantarum 115 (4):
571–576.
Kang, D.J., Seo, Y.J., Lee, J.D. et al. (2005). Jasmonic acid differentially affects growth, ion
uptake and abscisic acid concentration in salt-tolerant and salt-sensitive rice cultivars.
Journal of Agronomy and Crop Science 191 (4): 273–282.
Khan, W., Prithiviraj, B., and Smith, D.L. (2003). Photosynthetic responses of corn and soybean
to foliar application of salicylates. Journal of Plant Physiology 160 (5): 485–492.
Kim, E.H., Kim, Y.S., Park, S.H. et al. (2009). Methyl jasmonate reduces grain yield by
mediating stress signals to alter spikelet development in rice. Plant Physiology 149 (4):
1751–1760.
20. Reference 273
Klessig, D.F. and Malamy, J. (1994). The salicylic acid signal in plants. Plant Molecular Biology
26 (5): 1439–1458.
Kohlen, W., Charnikhova, T., Liu, Q. et al. (2011). Strigolactones are transported through the
xylem and play a key role in shoot architectural response to phosphate deficiency in
nonarbuscular mycorrhizal host Arabidopsis. Plant Physiology 155 (2): 974–987.
Koltai, H. (2011). Strigolactones are regulators of root development. The New Phytologist 190:
545–549.
Koornneef, M., Bosma, T.D.G., Hanhart, C.J. et al. (1990). The isolation and characterization
of gibberellin-deficient mutants in tomato. Theoretical and Applied Genetics 80 (6):
852–857.
Kurepin, L.V., Qaderi, M.M., Back, T.G. et al. (2008). A rapid effect of applied brassinolide on
abscisic acid concentrations in Brassica napus leaf tissue subjected to short-term heat stress.
Plant Growth Regulation 55 (3): 165–167.
Kwak, J.M., Mori, I.C., Pei, Z.M. et al. (2003). NADPH oxidase AtrbohD and AtrbohF genes
function in ROS-dependent ABA signaling in Arabidopsis. The EMBO Journal 22 (11):
2623–2633.
Lackman, P., González-Guzmán, M., Tilleman, S. et al. (2011). Jasmonate signaling involves
the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and
tobacco. Proceedings of the National Academy of Sciences of the United States of America
https://doi.org/10.1073/pnas.1103010108.
Larkindale, J. and Knight, M.R. (2002). Protection against heat stress-induced oxidative
damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant
Physiology 128 (2): 682–695.
Larkindale, J., Hall, J.D., Knight, M.R., and Vierling, E. (2005). Heat stress phenotypes of
Arabidopsis mutants implicate multiple signaling pathways in the acquisition of
thermotolerance. Plant Physiology 138 (2): 882–897.
Lehmann, J., Atzorn, R., Brückner, C. et al. (1995). Accumulation of jasmonate, abscisic acid,
specific transcripts and proteins in osmotically stressed barley leaf segments. Planta 197 (1):
156–162.
Li, L., Staden, J.V., and Jäger, A.K. (1998). Effects of plant growth regulators on the antioxidant
system in seedlings of two maize cultivars subjected to water stress. Plant Growth Regulation
25 (2): 81–87.
Li, J., Nam, K.H., Vafeados, D., and Chory, J. (2001). BIN2, a new brassinosteroid-insensitive
locus in Arabidopsis. Plant Physiology 127 (1): 14–22.
Li, Y.H., Liu, Y.J., Xu, X.L. et al. (2012). Effect of 24-epibrassinolide on drought stress-induced
changes in Chorispora bungeana. Biologia Plantarum 56 (1): 192–196.
Liu, Y., Zhao, Z., Si, J. et al. (2009). Brassinosteroids alleviate chilling-induced oxidative
damage by enhancing antioxidant defense system in suspension cultured cells of Chorispora
bungeana. Plant Growth Regulation 59 (3): 207–214.
Liu, J., He, H., Vitali, M. et al. (2015). Osmotic stress represses strigolactone biosynthesis in
Lotus japonicus roots: exploring the interaction between strigolactones and ABA under
abiotic stress. Planta 241 (6): 1435–1451.
Lopez-Raez, J.A., Kohlen, W., Charnikhova, T. et al. (2010). Does abscisic acid affect
strigolactone biosynthesis? The New Phytologist 187: 343–354.
21. 11 Role of Growth Regulators and Phytohormones in Overcoming Environmental Stress
274
Lorenzo, O. and Solano, R. (2005). Molecular players regulating the jasmonate signalling
network. Current Opinion in Plant Biology 8 (5): 532–540.
Magome, H., Yamaguchi, S., Hanada, A. et al. (2004). Dwarf and delayed-flowering 1, a novel
Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a
putative AP2 transcription factor. The Plant Journal 37 (5): 720–729.
Mahajan, S. and Tuteja, N. (2005). Cold, salinity and drought stresses: an overview. Archives of
Biochemistry and Biophysics 444 (2): 139–158.
Mason, H.S. and Mullet, J.E. (1990). Expression of two soybean vegetative storage protein
genes during development and in response to water deficit, wounding, and jasmonic acid.
The Plant Cell 2 (6): 569–579.
Mauch-Mani, B. and Mauch, F. (2005). The role of abscisic acid in plant–pathogen interactions.
Current Opinion in Plant Biology 8 (4): 409–414.
McConn, M., Creelman, R.A., Bell, E., and Mullet, J.E. (1997). Jasmonate is essential for insect
defense in Arabidopsis. Proceedings of the National Academy of Sciences of the United States
of America 94 (10): 5473–5477.
Merchan, F., Lorenzo, L.D., Rizzo, S.G. et al. (2007). Identification of regulatory pathways
involved in the reacquisition of root growth after salt stress in Medicago truncatula. The
Plant Journal 51 (1): 1–17.
Metwally, A., Finkemeier, I., Georgi, M., and Dietz, K.J. (2003). Salicylic acid alleviates the
cadmium toxicity in barley seedlings. Plant Physiology 132 (1): 272–281.
Miura, K. and Tada, Y. (2014). Regulation of water, salinity, and cold stress responses by
salicylic acid. Frontiers in Plant Science 5: 4.
Moons, A., Prinsen, E., Bauw, G., and Van Montagu, M. (1997). Antagonistic effects of abscisic
acid and jasmonates on salt stress-inducible transcripts in rice roots. The Plant Cell 9 (12):
2243–2259.
Morgan, P.W. and Drew, M.C. (1997). Ethylene and plant responses to stress. Physiologia
Plantarum 100 (3): 620–630.
Munne-Bosch, S. and Penuelas, J. (2003). Photo-and antioxidative protection, and a role for
salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants.
Planta 217 (5): 758–766.
Nakashita, H., Yasuda, M., Nitta, T. et al. (2003). Brassinosteroid functions in a broad range of
disease resistance in tobacco and rice. The Plant Journal 33 (5): 887–898.
Naqvi, S.S.M., Ansari, R., and Khanzada, A.N. (1982). Response of salt-stressed wheat
seedlings to kinetin. Plant Science Letters 26 (2-3): 279–283.
Navarro, L., Dunoyer, P., Jay, F. et al. (2006). A plant miRNA contributes to antibacterial
resistance by repressing auxin signaling. Science 312 (5772): 436–439.
Nazar, R., Iqbal, N., Syeed, S., and Khan, N.A. (2011). Salicylic acid alleviates decreases in
photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and
antioxidant metabolism differentially in two mungbean cultivars. Journal of Plant Physiology
168 (8): 807–815.
Nie, W.F., Wang, M.M., Xia, X.J. et al. (2013). Silencing of tomato RBOH1 and MPK2 abolishes
brassinosteroid-induced H2O2 generation and stress tolerance. Plant, Cell & Environment 36
(4): 789–803.
Nishiyama, R., Watanabe, Y., Fujita, Y. et al. (2011). Analysis of cytokinin mutants and
regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in
22. Reference 275
drought, salt and abscisic acid responses, and abscisic acid biosynthesis. The Plant Cell
https://doi.org/10.1105/tpc.111.087395.
Nunez, M., Mazzafera, P., Mazorra, L.M. et al. (2003). Influence of a brassinosteroid analogue
on antioxidant enzymes in rice grown in culture medium with NaCl. Biologia Plantarum 47
(1): 67–70.
O’donnell, P.J., Schmelz, E.A., Moussatche, P. et al. (2003). Susceptible to intolerance–a range
of hormonal actions in a susceptible Arabidopsis pathogen response. The Plant Journal 33
(2): 245–257.
Olszewski, N., Sun, T.P., and Gubler, F. (2002). Gibberellin signaling: biosynthesis, catabolism,
and response pathways. The Plant Cell 14 (suppl 1): S61–S80.
Pandey, A., Sharma, M., and Pandey, G.K. (2016). Emerging roles of strigolactones in plant
responses to stress and development. Frontiers in Plant Science 7: 434.
Parashar, A. and Varma, S.K. (1988). Effect of presowing seed soaking in gibberellic acid,
duration of soaking, different temperatures and their interaction on seed germination
and early seedling growth of wheat under saline conditions. Plant Physiology and
Biochemistry.
Paré, P.W. and Tumlinson, J.H. (1999). Plant volatiles as a defense against insect herbivores.
Plant Physiology 121 (2): 325–332.
Parihar, P., Singh, S., Singh, R. et al. (2015). Effect of salinity stress on plants and its tolerance
strategies: a review. Environmental Science and Pollution Research 22 (6): 4056–4075.
Pedranzani, H., Racagni, G., Alemano, S. et al. (2003). Salt tolerant tomato plants show
increased levels of jasmonic acid. Plant Growth Regulation 41 (2): 149–158.
Pei, Z.M., Murata, Y., Benning, G. et al. (2000). Calcium channels activated by hydrogen
peroxide mediate abscisic acid signalling in guard cells. Nature 406 (6797): 731.
Peleg, Z. and Blumwald, E. (2011). Hormone balance and abiotic stress tolerance in crop
plants. Current Opinion in Plant Biology 14 (3): 290–295.
Peleg, Z., Reguera, M., Tumimbang, E. et al. (2011). Cytokinin-mediated source/sink
modifications improve drought tolerance and increase grain yield in rice under water-stress.
Plant Biotechnology Journal 9 (7): 747–758.
Peng, Z.Y., Zhou, X., Li, L. et al. (2008). Arabidopsis hormone database: a comprehensive
genetic and phenotypic information database for plant hormone research in Arabidopsis.
Nucleic Acids Research 37 (suppl_1): D975–D982.
Pichersky, E. and Gershenzon, J. (2002). The formation and function of plant volatiles:
perfumes for pollinator attraction and defense. Current Opinion in Plant Biology 5 (3):
237–243.
Pospíšilová, J. (2003). Interaction of cytokinins and abscisic acid during regulation of stomatal
opening in bean leaves. Photosynthetica 41 (1): 49–56.
Pospisilova, J., Vagner, M., Malbeck, J. et al. (2005). Interactions between abscisic acid and
cytokinins during water stress and subsequent rehydration. Biologia Plantarum 49 (4):
533–540.
Prakash, L. and Prathapasenan, G. (1990). NaCl-and gibberellic acid-induced changes in the
content of auxin and the activities of cellulase and pectin lyase during leaf growth in rice
(Oryza sativa). Annals of Botany 65 (3): 251–257.
Rashotte, A.M., Carson, S.D., To, J.P., and Kieber, J.J. (2003). Expression profiling of cytokinin
action in Arabidopsis. Plant Physiology 132 (4): 1998–2011.
23. 11 Role of Growth Regulators and Phytohormones in Overcoming Environmental Stress
276
Ribaut, J.M. and Pilet, P.E. (1994). Water stress and indole-3ylacetic acid content of maize
roots. Planta 193: 502–507.
Roychoudhury, A. and Banerjee, A. (2017). Abscisic acid signaling and involvement of mitogen
activated protein kinases and calcium-dependent protein kinases during plant abiotic stress.
In: Mechanism of Plant Hormone Signaling Under Stress, vol. 1 (ed. G.K. Pandey), 197–241.
Hoboken, NJ: Wiley.
Roychoudhury, A. and Basu, S. (2008). Overexpression of an abiotic-stress inducible plant
protein in the bacteria Escherichia coli. African Journal of Biotechnology 7: 3231–3234.
Roychoudhury, A. and Paul, A. (2012). Abscisic acid-inducible genes during salinity and
drought stress. Advances in Medicine and Biology 51: 1–78.
Roychoudhury, A. and Sengupta, D.N. (2009). The promoter-elements of some abiotic stress-
inducible genes from cereals interact with a nuclear protein from tobacco. Biologia
Plantarum 53: 583–587.
Roychoudhury, A., Roy, C., and Sengupta, D.N. (2007). Transgenic tobacco plants
overexpressing the heterologous lea gene Rab16A from rice during high salt and water
deficit display enhanced tolerance to salinity stress. Plant Cell Reports 26: 1839–1859.
Roychoudhury, A., Basu, S., Sarkar, S.N., and Sengupta, D.N. (2008a). Comparative
physiological and molecular responses of a common aromatic indica rice cultivar to high
salinity with non-aromatic indica rice cultivars. Plant Cell Reports 27: 1395–1410.
Roychoudhury, A., Gupta, B., and Sengupta, D.N. (2008b). Trans-acting factor designated
OSBZ8 interacts with both typical abscisic acid responsive elements as well as abscisic acid
responsive element-like sequences in the vegetative tissues of indica rice cultivars. Plant Cell
Reports 27: 779–794.
Roychoudhury, A., Basu, S., and Sengupta, D.N. (2009a). Effects of exogenous abscisic acid on
some physiological responses in a popular aromatic indica rice compared with those from
two traditional non-aromatic indica rice cultivars. Acta Physiologiae Plantarum 31: 915–926.
Roychoudhury, A., Basu, S., and Sengupta, D.N. (2009b). Comparative expression of two
abscisic acid-inducible genes and proteins in the seeds of an aromatic indica rice cultivar
with that of non-aromatic indica rice cultivars. Indian Journal of Experimental Biology 47:
827–833.
Roychoudhury, A., Paul, S., and Basu, S. (2013). Cross-talk between abscisic acid-dependent
and abscisic acid-independent pathways during abiotic stress. Plant Cell Reports 32:
985–1006.
Roychoudhury, A., Ghosh, S., Paul, S. et al. (2016). Pre-treatment of seeds with salicylic acid
attenuates cadmium chloride-induced oxidative damages in the seedlings of mungbean
(Vigna radiata L. Wilczek). Acta Physiologiae Plantarum 38: 11.
Ruyter-Spira, C., Al-Babili, S., Van Der Krol, S., and Bouwmeester, H. (2013). The biology of
strigolactones. Trends in Plant Science 18 (2): 72–83.
Saeed, W., Naseem, S., and Ali, Z. (2017). Strigolactones biosynthesis and their role in abiotic
stress resilience in plants: a critical review. Frontiers in Plant Science 8: 1487.
Sakhabutdinova, A.R., Fatkhutdinova, D.R., Bezrukova, M.V., and Shakirova, F.M. (2003).
Salicylic acid prevents the damaging action of stress factors on wheat plants. Bulgarian
Journal of Plant Physiology 21: 314–319.
Santner, A., Calderon-Villalobos, L.I.A., and Estelle, M. (2009). Plant hormones are versatile
chemical regulators of plant growth. Nature Chemical Biology 5 (5): 301.
24. Reference 277
Sastry, E.V. and Shekhawat, K.S. (2001). Alleviatory effect of GA3 on the effects of salinity at
seedling stage in wheat (Triticum aestivum). Indian Journal of Agricultural Research 35 (4):
226–231.
Schwechheimer, C. (2008). Understanding gibberellic acid signalling—are we there yet?
Current Opinion in Plant Biology 11 (1): 9–15.
Seki, M., Narusaka, M., Ishida, J. et al. (2002). Monitoring the expression profiles of 7000
Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA
microarray. The Plant Journal 31 (3): 279–292.
Sembdner, G. and Parthier, B. (1993). The biochemistry and the physiological and molecular
actions of jasmonates. Annual Review of Plant Biology 44 (1): 569–589.
Senaratna, T., Tuochell, D., Bunn, T., and Dixon, K. (2000). Acetyl salicylic acid (aspirin) and
salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth
Regulation 30: 157–161.
Shirasu, K., Nakajima, H., Rajasekhar, V.K. et al. (1997). Salicylic acid potentiates an agonist-
dependent gain control that amplifies pathogen signals in the activation of defense
mechanisms. The Plant Cell 9 (2): 261–270.
Singh, V.P., Prasad, S.M., Munné-Bosch, S., and Müller, M. (2017). Phytohormones and the
regulation of stress tolerance in plants: current status and future directions. Frontiers in
Plant Science 8: 1871.
Skirycz, A., Claeys, H., De Bodt, S. et al. (2011a). Pause-and-stop: the effects of osmotic stress
on cell proliferation during early leaf development in Arabidopsis and a role for ethylene
signaling in cell cycle arrest. The Plant Cell https://doi.org/10.1105/tpc.111.084160.
Spollen, W.G., LeNoble, M.E., Sammuels, T.D., Bernstein, N., Sharp, R.E., 2000. Abscisic acid
accumulation maintains maize primary root elon gation at low water potentials by
restricting ethylene production. Plant Physiology 122: 967–976.
Stamm, P. and Kumar, P.P. (2010). The phytohormone signal network regulating elongation
growth during shade avoidance. Journal of Experimental Botany 61 (11): 2889–2903.
Stamm, P., Ravindran, P., Mohanty, B. et al. (2012). Insights into the molecular mechanism of
RGL2-mediated inhibition of seed germination in Arabidopsis thaliana. BMC Plant Biology
12 (1): 179.
Steber, C.M. and McCourt, P. (2001). A role for brassinosteroids in germination in Arabidopsis.
Plant Physiology 125 (2): 763–769.
Tari, I., Csiszár, J., Szalai, G. et al. (2002). Acclimation of tomato plants to salinity stress after a
salicylic acid pre-treatment. Acta Biologica Szegediensis 46 (3-4): 55–56.
Teale, W.D., Ditengou, F.A., Dovzhenko, A.D. et al. (2008). Auxin as a model for the integration
of hormonal signal processing and transduction. Molecular Plant 1 (2): 229–237.
To, J.P. and Kieber, J.J. (2008). Cytokinin signaling: two-components and more. Trends in Plant
Science 13 (2): 85–92.
Tran, L.S.P., Urao, T., Qin, F. et al. (2007). Functional analysis of AHK1/ATHK1 and cytokinin
receptor histidine kinases in response to abscisic acid, drought, and salt stress in
Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America
104 (51): 20623–20628.
Tsuchisaka, A. and Theologis, A. (2004). Unique and overlapping expression patterns among
the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant
Physiology 136 (2): 2982–3000.
25. 11 Role of Growth Regulators and Phytohormones in Overcoming Environmental Stress
278
Tuteja, N. (2007). Abscisic acid and abiotic stress signaling. Plant Signaling & Behavior 2 (3):
135–138.
Umehara, M., Hanada, A., Yoshida, S. et al. (2008). Inhibition of shoot branching by new
terpenoid plant hormones. Nature 455 (7210): 195.
Van Ha, C., Leyva-González, M.A., Osakabe, Y. et al. (2014). Positive regulatory role of
strigolactone in plant responses to drought and salt stress. Proceedings of the National
Academy of Sciences of the United States of America 111 (2): 851–856.
Vardhini, B.V. and Rao, S.S.R. (2003). Amelioration of osmotic stress by brassinosteroids on
seed germination and seedling growth of three varieties of sorghum. Plant Growth
Regulation 41 (1): 25–31.
Waldie, T., McCulloch, H., and Leyser, O. (2014). Strigolactones and the control of plant
development: lessons from shoot branching. The Plant Journal 79 (4): 607–622.
Wang, Y., Mopper, S., and Hasenstein, K.H. (2001). Effects of salinity on endogenous ABA,
IAA, JA, and SA in Iris hexagona. Journal of Chemical Ecology 27 (2): 327–342.
Wasternack, C. and Parthier, B. (1997). Jasmonate-signalled plant gene expression. Trends in
Plant Science 2 (8): 302–307.
Wickson, M. and Thimann, K.V. (1958). The antagonism of auxin and kinetin in apical
dominance. Physiologia Plantarum 11 (1): 62–74.
Wolters, H. and Jürgens, G. (2009). Survival of the flexible: hormonal growth control and
adaptation in plant development. Nature Reviews Genetics 10 (5): 305.
Xia, X.J., Wang, Y.J., Zhou, Y.H. et al. (2009). Reactive oxygen species are involved
in brassinosteroid-induced stress tolerance in cucumber. Plant Physiology 150 (2):
801–814.
Xia, X.J., Zhou, Y.H., Ding, J. et al. (2011). Induction of systemic stress tolerance by
brassinosteroid in Cucumis sativus. New Phytologist 191 (3): 706–720.
Xu, K., Xu, X., Fukao, T. et al. (2006). Sub1A is an ethylene-response-factor-like gene that
confers submergence tolerance to rice. Nature 442 (7103): 705.
Xue, L.W., Du, J.B., Yang, H. et al. (2009). Brassinosteroids counteract abscisic acid in
germination and growth of Arabidopsis. Zeitschrift für Naturforschung C 64 (3-4): 225–230.
Yamaguchi, S. (2008). Gibberellin metabolism and its regulation. Annual Review of Plant
Biology 59: 225–251.
Yamaguchi, S. and Kamiya, Y. (2000). Gibberellin biosynthesis: its regulation by endogenous
and environmental signals. Plant and Cell Physiology 41 (3): 251–257.
Yang, T. and Poovaiah, B.W. (2000). Molecular and biochemical evidence for the involvement
of calcium/calmodulin in auxin action. Journal of Biological Chemistry 275 (5): 3137–3143.
Yang, Z.M., Wang, J., Wang, S.H., and Xu, L.L. (2003). Salicylic acid-induced aluminum
tolerance by modulation of citrate efflux from roots of Cassia tora L. Planta 217 (1):
168–174.
Yang, X., Yang, Y.N., Xue, L.J. et al. (2011). Rice ABI5-like1 regulates ABA and auxin
responses by affecting the expression of ABRE-containing genes. Plant Physiology https://
doi.org/10.1104/pp.111.173427.
Yoneyama, K., Yoneyama, K., Takeuchi, Y., and Sekimoto, H. (2007). Phosphorus deficiency in
red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and
germination stimulant for root parasites. Planta 225 (4): 1031–1038.
26. Reference 279
Zahir, Z.A., Asghar, H.N., and Arshad, M. (2001). Cytokinin and its precursors for improving
growth and yield of rice. Soil Biology and Biochemistry 33 (3): 405–408.
Zhang, S., Cai, Z., and Wang, X. (2009a). The primary signaling outputs of brassinosteroids are
regulated by abscisic acid signaling. Proceedings of the National Academy of Sciences of the
United States of America 106 (11): 4543–4548.
Zhang, S.W., Li, C.H., Cao, J. et al. (2009b). Altered architecture and enhanced drought
tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3.
13 activation. Plant Physiology 151 (4): 1889–1901.
Zhang, A., Zhang, J., Zhang, J. et al. (2011). Nitric oxide mediates brassinosteroid-induced ABA
biosynthesis involved in oxidative stress tolerance in maize leaves. Plant and Cell Physiology
52 (1): 181–192.
Zhang, J.C., Yao, W., Dong, C. et al. (2015). Comparison of ketamine, 7, 8-dihydroxyflavone,
and ANA-12 antidepressant effects in the social defeat stress model of depression.
Psychopharmacology 232 (23): 4325–4335.
