Interactions of Brassinosteroids with Major Phytohormones: Antagonistic Effects

Abstract

Brassinosteroids (BRs) constitute an important class of signaling molecules capable of executing diverse functions ranging from plant growth, development, reproduction, and even stress tolerance. The recent literature on BRs has discussed these wide ranging roles and potentials of BRs. However, the maintenance of metabolic equivalents in the global context of other phytohormones is largely unknown. In this article, we have highlighted such interactive antagonistic cross-talks between BRs and other phytohormones which are crucial in growth regulation and abiotic stress tolerance. Such competitive interactions with BRs have been observed in the cases of abscisic acid, ethylene, auxin, gibberellins, salicylic acid, and even polyamines during physiological growth or abiotic stresses. The discussion largely presents the unique characters of plant molecular physiology and development regarding BR- and other phytohormone-mediated interactive antagonism. © 2018 Springer Science+Business Media, LLC, part of Springer Nature

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Journal of Plant Growth Regulation
https://doi.org/10.1007/s00344-018-9828-5
Interactions ofBrassinosteroids withMajor Phytohormones:
Antagonistic Effects
AdityaBanerjee1· AryadeepRoychoudhury1
Received: 3 March 2018 / Accepted: 25 June 2018
© Springer Science+Business Media, LLC, part of Springer Nature 2018
Abstract
Brassinosteroids (BRs) constitute an important class of signaling molecules capable of executing diverse functions ranging
from plant growth, development, reproduction, and even stress tolerance. The recent literature on BRs has discussed these
wide ranging roles and potentials of BRs. However, the maintenance of metabolic equivalents in the global context of other
phytohormones is largely unknown. In this article, we have highlighted such interactive antagonistic cross-talks between BRs
and other phytohormones which are crucial in growth regulation and abiotic stress tolerance. Such competitive interactions
with BRs have been observed in the cases of abscisic acid, ethylene, auxin, gibberellins, salicylic acid, and even polyamines
during physiological growth or abiotic stresses. The discussion largely presents the unique characters of plant molecular
physiology and development regarding BR- and other phytohormone-mediated interactive antagonism.
Keywords Brassinosteroids· Phytohormones· Plant growth regulators· Signaling· Antagonism· Cross-talk· Metabolic
homeostasis· Growth and development· Abiotic stress
Introduction
Brassinosteroids (BRs) form a novel group of phytohor-
mones. The members of this family of steroidal hormones
contain polyhydroxylated sterol structures (Grove etal.
1979). The name ‘brassinosteroids’ can be attributed to
the initial identification of these compounds in the pollen
grains of Brassica napus. The first identified BR was named
‘brassinolide’ (Grove etal. 1979). Previous investigations
have validated the potential role of BRs in regulating diverse
physiological processes like germination, cell growth and
senescence, differentiation of the vascular tissues, floral
reproduction, and even abiotic and biotic stress responses
(Sharma etal. 2015; Vardhini and Anjum 2015; Tang etal.
2016; Wei and Li 2016; Xia etal. 2014, 2009a, b; Zhang
etal. 2008; Bajguz and Hayat 2009).
Biosynthesis of brassinolide (BL) is initiated from the
precursor compound, campesterol via recurring reduc-
tions, hydroxylations, epimerizations, and oxidations
(Fujioka etal. 1998; Fujioka and Yokota 2003). The
other major BRs are synthesized via the mevalonic acid-
dependent triterpenoid pathway (Chung and Choe 2013).
In this pathway, campesterol is modified by enzymes like
C-22 hydroxylase dwarf4/CYP90B1 (DWF4) and C-3
hydrogenase constitutive photomorphogenesis and dwarf/
CYP90A1 (CPD) (Chung and Choe 2013; Bajguz 2007).
The biosynthesis is regulated by controlling the expression
of anabolic genes [DWF4, CPD, 5α-reductase: de-etio-
lated-2 (DET2), C-22 hydroxylase: rotundifolia/CYP90C1
(ROT3)] or by reducing the levels of bioactive BR (Guo
etal. 2013; Vriet etal. 2013; Clouse 2015). BR-mediated
signaling is positively regulated by basic helix-loop-helix
(bHLH) transcription factors (TFs) like CESTA and TCP
(Poppenberger etal. 2011). Saini etal. (2015) reported that
abscisic acid (ABA)-dependent factors like ABA insensi-
tive 3/viviparous1 (ABI3/VP1) and related to ABI3/VP1
(RAV1) positively regulated BR biosynthesis by inducing
the expression of BR insensitive 1 (BRI1), the BR recep-
tor in rice. It was found that the plants with mutations in
the BRI1 gene exhibited high accumulation of BRs due
to loss of feedback regulation (Sun etal. 2010; Cano-
Delgado etal. 2004; Karlova etal. 2006). On association
with the co-receptor BRI1 ASSOCIATED RECEPTOR
KINASE 1 (BAK1), BRI1 is serially phosphorylated and
* Aryadeep Roychoudhury
aryadeep.rc@gmail.com
1 Post Graduate Department ofBiotechnology, St. Xavier’s
College (Autonomous), 30, Mother Teresa Sarani, Kolkata,
WestBengal700016, India

Journal of Plant Growth Regulation
1 3
de-phosphorylated (Li etal. 2002; Nam and Li 2002). This
promotes BR-mediated signal transduction and regulation
of physiologically crucial genes via TFs (Nakamura etal.
2017). Symons etal. (2008) presented important obser-
vations regarding BR signaling. They observed that BRs
are utilized in close proximity of the synthesizing cells
via conjugates and specific transporters. However, the
long distance effects of BRs are exerted through exten-
sive cross-talks with multiple phytohormones (Vriet etal.
2013; Gudesblat and Russinova 2011). This article aims at
presenting an exhaustive discussion regarding the antago-
nistic metabolic interactions between BRs and other phy-
tohormones during developmental growth or under various
abiotic stress responses. Illustration of the above conse-
quences in this review can be useful for understanding
the BR-mediated dynamics in diverse plant physiological
responses.
BRs andPlant Growth Regulation
Diverse species ranging from higher plants to the monoplast
freshwater algae and brown algae have been reported to pro-
duce BRs. In higher plants, the highest BR accumulation
was detected in immature seeds, roots, flowers, and pollens.
However, shoots and leaves accumulated lower amounts
of BRs (Kutschera and Wang 2012; Takatsuto 1994). BRs
exhibit autocrine and paracrine functioning. Hence, passive
and active intracellular transport are required for the effec-
tive mobilization of BRs from the site of synthesis to the cell
membrane and early endosomal compartments (Tang etal.
2016). The production of BRs and their receptor-dependent
signaling influence cell division and leaf expansion. Arabi-
dopsis mutants, constitutive photomorphogenesis and dwarf-
ism (cpd) deficient in BRs exhibited reduced leaf blades
and thwarted cell division (Noguchi etal. 1999). Several
cyclin-dependent kinase (CDK) encoding genes like CYCA,
CYCB, CYCD3;1, CYCD3;2, and cyclophilins are regulated
by BRs (Fu etal. 2008). Sun etal. (2015) reported the regu-
latory expression of U-type cyclin CYC U4;1 and glyco-
gen synthase kinase by the TF, BRI1-EMS-SUPPRESSOR
1 (BES1) in rice. This reduces the cellular proliferation in
the abaxial sclerenchyma to promote leaf erectness. BRs
are involved in regulating diverse physiological parameters
like source-sink relationships, germination, photosynthe-
sis, senescence, photomorphogenesis, and flowering (Var-
dhini and Anjum 2015). Recent data suggest the immense
roles of BRs in maintaining meristem size, hair formation,
and lateral root growth (Wei and Li 2016). Identifying the
involvement of various phytohormones in such BR-mediated
growth responses can provide valuable insights into the sys-
temic physiology of plant growth.
BRs andAbiotic Stresses
Abiotic stresses like salinity, drought, temperature, light,
and heavy metal toxicity are major agricultural challenges.
These edaphic and atmospheric stresses account for a large
proportion of global crop losses (Banerjee etal. 2017).
The antagonistic cross-interactions between BRs and the
growth regulating phytohormones like ABA, ethylene, sal-
icylic acid (SA), auxin, gibberellins, and polyamines can
reveal potential molecular targets which can be genetically
manipulated to generate tolerance (Vardhini and Anjum
2015). It has been noted that such antagonistic cross-
talks actually balance plant growth and survival during
abiotic stresses. Accounting for the diverse physiological
functions of BRs, this group of phytohormones can be
promoted as crucial growth regulators essential for plant
development (Divi and Krishna 2009).
Abiotic stresses severely retard plant systemic devel-
opment by inhibiting the cell cycle and disrupting the
cellular architecture. Both control and stress conditions
induce the BR-dependent TF, BRASSINAZOLE RESIST-
ANT 1 (BZR1) to maintain normal progression of the cell
cycle (Hacham etal. 2011). The R2R3 MYB TF, BRASSI-
NOSTEROIDS AT VASCULAR AND ORGANIZING
CENTER (BRAVO) inhibits cellular proliferation of plant
stem cells (quiescent center cell). Interaction with BES1
represses the activity of BRAVO and initiates cell division
in the root QC (Vilarrasa-Blasi etal. 2014). This mecha-
nism promotes plant longevity and stress adaptation.
Recently, Rao and Dixon (2017) inferred that BRs
manipulate cell wall remodeling in members of the
Poaceae family during abiotic stresses. Genes encoding
cell wall remodeling enzymes, that is, pectin lyase like
(PLLs), expansins (EXPs), and xyloglucan endotrans-
glucosylase/hydrolases (XTHs) are induced by BRs (Rao
and Dixon 2017). The expression of EXPs and endoglu-
canases (GLUs) in rice was found to be regulated by BES1
via a cross-talk between phytohormones (Schmidt etal.
2013). Loss of integrity in the Arabidopsis cell wall dur-
ing abiotic stresses is resisted by the stimulation of the
BRI1 receptor which up-regulates the expression of genes
encoding pectin methyl esterases (PMEs). The cell wall is
maintained through an integrated hormonal outplay gener-
ated by the interaction of BAK1 and RECEPTOR-LIKE
PROTEIN (RPL44) (Wolf etal. 2014).
Some available reports have identified the roles of
BRs during abiotic stress responses. Tiwari etal. (2017)
proposed active participation of BRs in drought stress
responses and tolerance. Overexpression of the BR biosyn-
thetic gene (encoding a cytochrome p450) CYP85A1 from
Spinacia oleracea conferred drought tolerance in trans-
genic tobacco plants (Duan etal. 2017). The transgenics

Journal of Plant Growth Regulation
1 3
accumulated lower levels of reactive oxygen species (ROS)
and malondialdehyde (MDA) along with higher levels of
proline and antioxidant enzymes compared to the wild
type plants (Duan etal. 2017). In an interesting finding,
it was observed that the WRKY TFs, that is, WRKY46,
WRKY54, and WRKY70 synchronizes with BES1 to
promote BR-induced plant growth by down-regulating
the drought stress-induced genes (Chen and Yin 2017).
Ahammed etal. (2015) reported significant reduction in
photoinhibition in tomato plants exogenously treated with
BRs. The plants exhibited increased quantum efficiency
of PSII and photochemical quenching coefficient. Inhibi-
tion of BR biosynthesis by brassinozole reduced the lev-
els of RuBisCO and other photosynthetic proteins (Xia
etal. 2009a). Vicia faba plants treated with BRs recorded
improved stomatal closure by reducing K+ uptake in the
guard cells (Haubrick etal. 2006). The mitigating roles of
BRs in plants exposed to high temperature, low tempera-
ture as well as freezing have been observed (Zhang etal.
2013; Janeczko etal. 2011, 2009; Wang etal. 2014). BRs
also ameliorate light stress in plants (Vardhini and Anjum
2015). The antioxidant machinery in Brassica juncea
exposed to zinc (Zn)- and chromium (Cr)-metal stress was
activated by the application of 24-epibrassinolide (Arora
etal. 2010a, b). Anuradha and Rao (2007a, b) showed the
ameliorative effects of 24-epibrassinolide in radish seed-
lings exposed to lead (Pb) and cadmium (Cd)-mediated
heavy metal toxicity.
Compatible solutes like proline, glycine betaine, fructans,
myo-inositol, soluble sugars, and so on are essential for
the maintenance of cellular equilibria during sub-optimal
conditions (Roychoudhury etal. 2015; Roychoudhury and
Banerjee 2016). Accumulation of BRs has often been asso-
ciated with increased cellular content of osmolytes (Kumar
etal. 2013). BR accumulation suppresses the phosphoryla-
tion activity of the glycogen synthase kinase-3-like kinase,
BRASSINOSTEROID INSENSITIVE 2 (BIN2). This main-
tains the TF, YODA (YDA) in an inactive form leading to
the activation of a mitogen-activated protein kinase (MAPK)
cascade which negatively regulates the stomatal develop-
ment (Kim etal. 2012). It was observed that the signaling
mutants, bin-2 and the BR biosynthetic mutants, det-2 exhib-
ited salt hypersensitivity and suppression of the proline ana-
bolic gene, Δ1-pyrroline-5-carboxylate synthase 1 (P5CS1)
(Zeng etal. 2010).
Cross‑Talk Between Brassinosteroids
andOther Phytohormones
Phytohormones are the most important signaling mediators
in plants. They regulate diverse stress responses by modu-
lating the entire signalosome. BRs are being regarded as a
novel class of signaling molecules involved in regulating
abiotic stress responses by interacting with multiple conven-
tional phytohormones (Sharma etal. 2017). The underlying
section highlights the antagonistic interactions between BR
and other phytohormone-mediated signaling.
Antagonistic Interactions Between BRs andABA
ABA is regarded as the universal stress phytohormone
which maintains embryo dormancy during seed maturation
(Roychoudhury and Banerjee 2017). Because BRs promote
seed germination, their antagonistic interaction with ABA
is evident (Hu and Yu 2014). ABA- and BR-mediated co-
regulation of several genes have been documented through
genetic and physiological studies (Nemhauser etal. 2006;
Zhang etal. 2009). Detailed analysis of BR mutants like
det-2 and bri-1 revealed that BIN2 negatively regulates BR
signaling after perceiving ABA-mediated molecular signal-
ing. However, studies in ABA signaling mutants highlighted
the participation of PP2C family of Ser/Thr phosphatases,
ABI1 and ABI2 in BR signaling (Zhang et al. 2009).
These enzymes act downstream of the receptor, BRI1, and
upstream of BIN2 to suppress BR signaling (Zhang etal.
2009). Recently, Wang etal. (2018) established that ABI1
and ABI2 interact with BIN2 to dephosphorylate it. Such
ABA-mediated regulation inhibits BIN2-induced phos-
phorylation of BES1 and thus dampens the BR-mediated
signaling (Fig.1). A concise signaling module consisting of
PP2Cs-BIN2-SnRK kinases has been highlighted, because
BIN2 suffices the feedback regulatory mode to phospho-
rylate SnRKs. This activates the ABA-dependent signaling
and suppresses BR-mediated molecular transduction (Wang
etal. 2018).
In another study, it was reported that BIN2 interacts and
phosphorylates ABI5. This activates the TF which medi-
ates ABA responses to restrict seed germination (Hu and
Yu 2014). Exogenous BR destabilizes the synergistic asso-
ciation between BIN2 and ABI5 and releases the ABA-
mediated inhibition of BR signaling (Hu and Yu 2014). Low
amounts of BR induce the genes encoding RESPIRATORY
BURST OXIDASE HOMOLOG (RBOH) to transiently pro-
duce low amounts of hydrogen peroxide (H2O2). This equili-
brates the cellular redox status by balancing glutathione and
also promotes BR-induced stomatal opening. High concen-
trations of BRs are maintained during stress as a result of
which prolonged H2O2 production activates ABA-dependent
signaling to stimulate stomatal closure (Xia etal. 2014).
A significant correlation between BR and ABA has been
observed during heat stress. High accumulations of BRs
and HEAT SHOCK PROTEIN 90 (HSP90) were observed
in the ABA biosynthetic mutant, aba1-1 exposed to heat
stress (Divi etal. 2010). Up-regulation of the gene encod-
ing BRASSINOSTEROID-SIGNALING KINASE 5 (BSK5)

Journal of Plant Growth Regulation
1 3
was observed in Arabidopsis plants treated with both ABA
and BR. BSK5 was found to be a crucial modulator of the
ABA signaling pathway, as the Arabidopsis bsk5 mutants
exhibited higher expression of ABA anabolic genes, ABA3
and 9-cis-epoxycarotenoid dioxygenase 3 (NCED3) (Li etal.
2012a, b). The cross-talk between BRs and ABA has also
been reported to be regulated by the TF, BZR1 (Yang etal.
2016). The bzr1-1D Arabidopsis mutants exhibited less
sensitivity to the ABA-induced inhibition on the growth of
primary roots. BZR1 also confers ABA hyposensitivity by
associating with the G-boxes in the ABI5 promoter and sup-
pressing ABI5 gene expression (Yang etal. 2016).
Antagonistic Interactions Between BRs andEthylene
The gaseous hormone, ethylene, is noted for its roles in fruit
ripening and gravitropic reorientations in seedlings. The
latter function of ethylene has large implications during
desiccation stress (Vandenbussche etal. 2013). BRs on the
contrary negatively regulate shoot gravitropism. As a result,
the outcome of ethylene and BR interactions influences the
auxin signaling genes to control gravitropic responses in
shoots (Guo etal. 2008). Unlike BRs, ethylene represses
the expression of the AUX/IAA genes which negatively regu-
late auxin signaling. This promotes the expression of auxin
responsive factor 7 (ARF7) and ARF19 (Fig.1). These genes
encode positive regulators of auxin signaling which mediate
gravitropic responses in the shoots (Vandenbussche etal.
2013). Similar ethylene-BR antagonism has been observed
during root gravitropic responses, where ethylene suppresses
the effect and BRs promote it (Buer etal. 2006).
The receptor-like kinase, FERONIA, is quintessential for
pollen tube reception and cellular elongation (Deslauriers
and Larsen 2010). The Arabidopsis knockout mutants of this
gene exhibited BR hyposensitivity (Guo etal. 2009). It was
reported that the ethylene-dependent growth of hypocotyls in
etiolated seedlings was antagonized by FERONIA-mediated
BR responses (Deslauriers and Larsen 2010). Interestingly,
exogenous application of BRs up-regulated the expression of
the ethylene biosynthetic gene, 1-aminocyclopropane-1-car-
boxylate synthase (ACS) (Muday etal. 2012). Ubiquitination
of ACS5, ACS6, and ACS9 by the 26S proteasome was also
stalled by BRs (Hansen etal. 2009).
In another report, ethylene and BRs were suggested to
antagonistically regulate alternative oxidase (AOX) activ-
ity during fruit ripening in Carica papaya (Mazorra etal.
2013). The AOX activity is responsive to changes in the
electron transport chain (ETC), phytohormone-mediated
signals, ROS, and metabolites associated with respira-
tion (Vanlerberghe 2013). The AOX capacity increased
both upon the exogenous application of 24-epibrassinolide
(epiBR) and even Brz2001 (BR biosynthetic inhibitor).
The ethylene emission rate remained constant for the initial
24h and then decreased on the fifth day of Brz treatment.
Application of the ethylene inhibitor, 1-methylcyclopropene
(1-MCP) reversed the results obtained by epiBR and Brz
treatments without 1-MCP. As a result, papaya fruits treated
with 1-MCP and epiBR exhibited suppressed AOX activ-
ity, thus highlighting the antagonistic competition occurring
between ethylene and BRs (Mazorra etal. 2013). Zhu etal.
(2016) identified the interaction between BRs and ethylene
in the fruits of tomato plants exposed to salt stress. H2O2 was
found to mediate the above cross-talk, since application of
a ROS scavenger or inhibitor of ROS synthesis significantly
blocked BR-induced ethylene production. Under condi-
tions of reduced ethylene production via use of 1-MCP, the
BR-induced tolerance to salt stress was reversed (Zhu etal.
2016). This indicates that in tomato plants, ethylene prob-
ably acts downstream of BRs to mediate salt stress tolerance.
Antagonistic Interactions Between BRs andAuxin
Plant adaptation and growth during abiotic stresses are
mediated via a complex redox signaling module formed by
auxin, ROS, antioxidants, glutathione (GSH), and associated
Fig. 1 An overview of some antagonistic cross-talks occurring
between BRs and phytohormones. In the presence of ABA, ABI1
and ABI2 dephosphorylate the BR-induced kinase BIN2. As a result,
BIN2 remains inactivated and cannot phosphorylate BES1, resulting
in suppressed BR-responsive signaling in the presence of ABA. BIN2
also interacts with the pathogenesis receptor, NPR1, which activates
the downstream TF, WRKY70 (a negative regulator of SA biosyn-
thesis). BRs suppress multiple PIN and LAX genes involved in auxin
transport. On the contrary, the AUX/IAA genes are up-regulated, lead-
ing to the elevated expression of ARF7 and ARF19. This promotes
auxin-dependent gravitropism which is usually repressed by ethylene.
Differential accumulation of PAs has also been observed. BRs inhibit
the accumulation of cadaverine and promote putrescine and spermi-
dine synthesis during abiotic stresses. Because PA biosynthesis is
positively linked to ABA-dependent transduction, such BR-mediated
regulation can be another unidentified tripartite node of BR–ABA–
PA signaling

Journal of Plant Growth Regulation
1 3
proteins. Auxin homeostasis directly regulates plant growth
plasticity during responses to stresses like temperature,
desiccation, and salinity (Salopek-Sondi etal. 2017). The
antagonism between auxin and BRs dictates the develop-
ment of an exaggerated apical hook in Arabidopsis seed-
lings grown under both light and dark conditions (Grauwe
etal. 2005). Exogenous application of BRs suppressed
auxin transport and formation of the apical hook (Grauwe
etal. 2005; Gruszka etal. 2016). Some of the pinformed
(PIN) genes (PIN2 and PIN5b) associated with auxin trans-
port were up-regulated by heat, cold, and drought stresses,
whereas the expression of other PIN genes remained sup-
pressed (Saini etal. 2015). BR down-regulated the expres-
sion of PIN3, PIN4, PIN7, and like auxin-resistant-1 (LAX)
genes (Fig.1). This pointed towards the existence of BR-
auxin cross-talk during abiotic stress (Nemhauser etal.
2004). Drought stress in rice down-regulated the expression
of all six YUCCA genes (encoding rate limiting enzymes
in the auxin biosynthetic pathway) except OsYUCCA4 (Du
etal. 2013). Interestingly, cold stress induced OsYUCCA2,
OsYUCCA3, OsYUCCA6, and OsYUCCA7. Again, heat
stress strongly up-regulated OsYUCCA3, OsYUCCA6, and
OsYUCCA7 genes (Du etal. 2013). The yucca rice mutants
exhibited altered profile of BR-induced genes which con-
firmed YUCCA-mediated auxin-BR cross-talk during abi-
otic stresses.
Proper root growth requires proper co-ordination between
auxin and BRs. Elevated levels of auxin and BZR1 are main-
tained by steady BR catabolism in the Arabidopsis roots.
This equilibrates the spatio-temporal balance of stem cell
dynamics required for optimum root and shoot growth. The
genes facilitating the elongation of the transition zone are
up-regulated by BZR1 (Chaiwanon and Wang 2015). BR
represses BRAVIS RADIX (BRX) required for root growth,
whereas auxin induces the same (Mouchel etal. 2006).
Zhang etal. (2014) detected reduced free indole acetic acid
(IAA) content in the joints of lamina in rice plants overex-
pressing OsARF19 and OsBRI1. OsARF19 was also found
to bind to the OsBRI1 promoter and positively regulate its
expression. However, in spite of activating BR signaling,
excess ARF19 reduced cellular IAA content via a feedback
regulation (Zhang etal. 2014).
Antagonistic Interactions Between BRs
andGibberellins
Gibberellic acid (GA) is a crucial growth-promoting hor-
mone which stimulates seed germination and internodal
elongation. Abiotic stress conditions usually promote the
accumulation of ABA, which in turn suppresses GA biosyn-
thesis. BRs dampen GA-mediated responses by maintaining
high cellular concentration of GA inhibitors like DELLA
and SLR1 (De Vleesschauwer etal. 2012). As a result,
the GA biosynthetic genes, GA20 oxidase (GA20ox) and
GA3ox3, are repressed and the GA catabolic gene, GA2ox is
induced (De Vleesschauwer etal. 2012) (Fig.1). Exogenous
treatment with high concentration of BRs activated GA2ox-3
and inhibited cell elongation. It has been shown that GAs
repress BR biosynthesis via feedback regulation, but activate
GA-mediated primary signaling to promote cell elongation
(Tong etal. 2014). Internodal cellular elongation promoted
by GAs requires BR signaling (Janeczko etal. 2016). The
tripartite BR-auxin-GA antagonism has been observed dur-
ing fiber initiation in cotton plants, Gossypium hirsutum
(Hu etal. 2011). BR and auxin treatments down-regulated
the DELLA gene GAII, whereas GA application induced
GAI1 and GAI3 during initiation of cotton fibers (Hu etal.
2011). In another study, it was found that the TFs, BZR1 and
REPRESSOR OF GAL-3 (RGA) antagonized their mutual
transcriptional activities to mediate positive and negative
regulation of BR and GA signaling, respectively (Li etal.
2012a, b; Ross 2016).
Antagonistic Interactions Between BRs andSalicylic
Acid (SA)
SA, mainly known for its roles in systemic acquired resist-
ance (SAR) during biotic stresses, also participates in abiotic
stress responses (Roychoudhury etal. 2016). WRKY70, the
major TF acting downstream of the non-expressor of patho-
genesis-related genes 1 (NPR1) mediates BR-SA cross-talk
(Divi etal. 2010). Interestingly, the Arabidopsis npr1-1
mutants were highly sensitive to heat stress and also exhib-
ited abnormal expression of the pathogenesis-related (PR)
genes in response to SA application (Larkindale etal. 2005).
It has been hypothesized that NPR1 regulates stress toler-
ance by interacting with BIN2 and BZR1 (Divi etal. 2010)
(Fig.1). The exact type of interaction in this case is not
known. WRKY70 negatively regulates SA biosynthesis (Li
etal. 2013). Hence, high expression of NPR1 during stress
probably induces BR signaling by repressing SA anabolism.
Interactions Between BRs andPolyamines
Polyamines (PAs) consist of an important class of compat-
ible solutes that maintain the cellular osmoticum in almost
all types of abiotic stresses (Banerjee and Roychoudhury
2018). Liu and Moriguchi (2007) suggested the interaction
of BRs and PAs in enhancing the systemic tolerance poten-
tial. Exogenous application of BRs increased endogenous
free PA content and ameliorated Cu stress in Raphanus
sativus L. cv. ‘Pusa chetki’ seedlings (Choudhary etal.
2010). The antagonistic action of BRs was observed on
cadaverine (higher PA) which promotes ROS production.
Exogenous application of BRs reduced the endogenous
content of cadaverine. However, the content of other PAs

Journal of Plant Growth Regulation
1 3
like spermidine and putrescine (required for the growth and
abiotic stress tolerance in plants) increased significantly
after BR treatment (Takahashi and Kakehi 2010) (Fig.1).
Co-application of BR and spermidine promoted tolerance
against Cu stress by modulating the ABA and auxin-depend-
ent signaling pathways (Choudhary etal. 2012).
Conclusion
BRs consist of a group of versatile phytohormones which
have significantly emerged in the context of the plant signa-
losome due to diverse functions in developmental growth
and stress responses. This minireview concisely illustrates
the situation- and stimulus-specific dynamic shifts in the
plant metabolome to balance BR-mediated signaling with
other phytohormones (Fig.1). The action of BRs is strictly
antagonistic to ABA, the most important stress hormone.
Tripartite interactions among BRs, ethylene, and auxin dis-
played the nodal factors responsible for maintaining plant
metabolism under myriad conditions. The roles of GA and
SA during abiotic stress are well determined. The antagonis-
tic interactions of these phytohormones with BRs open up a
new avenue of studying stress physiology. The involvement
of stress regulators like NPR1 and WRKY70 in SA and BR
signaling presented a novel interaction of these hormones
under both abiotic and biotic stress conditions.
Future Perspectives
Plant signaling in the context of BR-induced responses is
still not well deciphered. The synergistic and antagonistic
cross-talks of all the phytohormones in a tissue-specific
pattern and under each isolated condition need to be docu-
mented. PAs are yet to be completely recognized as phyto-
hormones, but their potential role in generating abiotic stress
tolerance and proposed cross-talk with BR-mediated signal-
ing during abiotic stress is important. This would facilitate
the complete understanding of systemic signaling. The role
of epigenetics in phytohormone-BR antagonism is predicted,
but largely unknown. Genome-wide epigenetic studies along
with next-generation sequencing of the transcriptome under
BR-treated conditions can be novel approaches for under-
standing the overall signaling induced by BRs. Such strate-
gies would also be crucial to sieve out, identify, and validate
potential molecular targets that can be genetically altered to
confer abiotic stress tolerance in transgenics.
Acknowledgements Financial support from Council of Scientific and
Industrial Research (CSIR), Government of India through the research
Grant [38(1387)/14/EMR-II] to Dr. Aryadeep Roychoudhury is grate-
fully acknowledged. The authors thank University Grants Commission,
Government of India for providing Junior Research Fellowship to Mr.
Aditya Banerjee.
Compliance with Ethical Standards
Conflict of interest The authors declare that they have no conflict of
interest.
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