TRPLSC-983; No.

of Pages 12

Review

Benefits of brassinosteroid crosstalk

Sikander Pal Choudhary1,2, Jing-Quan Yu1, Kazuko Yamaguchi-Shinozaki3,
Kazuo Shinozaki4 and Lam-Son Phan Tran5
1
Department of Horticulture, Zhejiang University, Hangzhou 310058, China
2
Department of Botany, University of Jammu, Jammu 180003, India
3
Japan International Research Center for Agricultural Sciences, Tsukuba, Ibaraki 305-8686, Japan
4
Gene Discovery Research Group, Plant Science Center, RIKEN Yokohama Institute, 1-7-22, Suehiro-cho, Tsurumi,
Yokohama 230-0045, Japan
5
Signaling Pathway Research Unit, Plant Science Center, RIKEN Yokohama Institute, 1-7-22, Suehiro-cho, Tsurumi,
Yokohama 230-0045, Japan

Brassinosteroids (BRs) are a group of phytohormones
that regulate various biological processes in plants.
Interactions and crosstalk between BRs and other plant
hormones control a broad spectrum of physiological and
developmental processes. In this review, we examine
recent findings which indicate that BR signaling compo-
nents mainly interact with the signaling elements of
other hormones at the transcriptional level. Our major
challenge is to understand how BR signaling indepen-
dently, or in conjunction with other hormones, controls
different BR-regulated activities. The application of a
range of biotechnological strategies based on the mod-
ulation of BR content and its interplay with other plant
growth regulators (PGRs) could provide a unique tool for
the genetic improvement of crop productivity in a sus-
tainable manner.
BRs regulate plant growth and stress responses
Over the past decade, extensive research efforts have
characterized all components of the BR signal relay from
the site of its perception to the ultimate point of the
regulation of gene expression. Intensive genetic and bio-
chemical strategies have been used to elucidate the com-
plete core of the BR signaling cascade [1,2]. In the past few
years, the BR metabolism and signaling pathway have
become a major focus of plant biology research [1,3]. Recent
studies have demonstrated the significance of BR homeo-
stasis for maintaining normal plant growth [2,4]. Crosstalk
and interactions between BRs and other PGRs occur
through either the modification or intersection of their
primary signaling cascades and function to regulate a large
and diverse array of biological processes [5–10]. In turn,
the execution of such a myriad of activities depends on BR
signal integration with various transcription factors (TFs)
that are implicated in the regulation of several develop-
mental and physiological processes, including responses to
abiotic and biotic stresses [6]. Synergistic BR and auxin
(Aux) actions have been attributed to their signaling ele-
ments, such as BRI1 and ARF2 (see Glossary) [2,6].
Recently, BR signaling components have been shown to
play a role in innate immunity and stomatal development
in Arabidopsis thaliana [11–14]. BRs have also been demon-
strated to regulate biotic and abiotic stress responses in
Corresponding author: Tran, L S (tran@psc.riken.jp).
1360-1385/$ – see front matter ß 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2012.05.012 Trends in Plant Science xx (2012) 1–12
plants [14–21]. In recent years, there has been a major
increase in the utilization of BRs in agricultural applica-
tions as a means to boost crop productivity and stress
tolerance [15–18,22]. In this review, we highlight the most
recent advances regarding our understanding of BR
metabolism and BR signaling. In addition, we examine
the roles played by BRs, either alone or in cooperation with
other PGRs, such as abscisic acid (ABA), Aux, cytokinins
(CKs), ethylene (ET), jasmonic acid (JA), salicylic acid (SA)
and gibberellins (GAs), in plant growth and development
and in abiotic and biotic stress responses. Furthermore, we
will also briefly discuss the implications of this knowledge
for plant biotechnology.
BR metabolism, perception and the execution of BR
signaling
BR metabolism
BR metabolism encompasses the synthesis of bioactive
BRs to conversions, modifications or the addition of side
chains resulting in the change of bioactive BRs to biologi-
cally inactive forms [1,23–25]. Various enzymatic steps in
BR biosynthesis and catabolism, such as glycosylation,
hydroxylation and sulfonation, are depicted in Figure 1.
Perception and execution of BR signaling
The signal transduction of BRs has been extensively stud-
ied. In plants, the BR signaling cascade involves the per-
ception of the BR signal and further downstream relay of
events leading to BR-induced gene expression [1–3,26–30]
(Figure 2). The BR signal is perceived by BRI1, a leucine-
rich repeat (LRR) receptor-like kinase (RLK), which func-
tions with its coreceptor BAK1/SERK3 in BR signaling.
BRI1 has a large extracellular ligand-binding domain of 25
LRRs and a 70-amino acid island domain between LRR20
and LRR21, a transmembrane domain and a cytoplasmic
domain with kinase activity [1,3]. In addition to its role in
BR signaling, BAK1 is also involved in light signaling, cell
death control and innate immunity [11,12,14,31]. The
SERK1, SERK2 and SERK4 also participate in the early
steps of BR signaling [32]. In the absence of BRs, BRI1
remains an inactive homodimer owing to an interaction
between its cytoplasmic domain and the negative regulator
BKI1, preventing the heterodimerization of BRI1 with
BAK1 [1,2,33]. In the presence of BRs, BR binding at
1
TRPLSC-983; No. of Pages 12
Review
Glossary
14-3-3 proteins: conserved regulatory proteins found in all the eukaryotic
cells.
ABI1 (ABSCISIC ACID-INSENSITIVE 1): a gene encoding a protein phosphatase
2C involved in abscisic acid (ABA) signal transduction.
ABI2 (ABA-INSENSITIVE 2): An ABI1 homologous gene encoding a protein
phosphatase 2C involved in ABA signal transduction.
ACC: 1-aminocyclopropane-1-carboxylic acid.
ACC oxidase: catalyzes the formation of ethylene from ACC.
ACS (ACC SYNTHASE): enzyme involved in ethylene synthesis.
ARF (AUXIN RESPONSE FACTOR): transcription factor regulating auxin-
mediated transcriptional activation–repression.
AtIWS (Arabidopsis thaliana INTERACT-WITH-SPT6): an evolutionarily con-
served protein involved in RNA polymerase II (RNAPII) post-recruitment and
transcriptional elongation processes.
BAK1 (BRI1-ASSOCIATED RECEPTOR KINASE 1): also known as SERK3, a
member of the somatic embryogenesis receptor kinase (SERK) family, acting
as a coreceptor of BRASSINOSTEROID INSENSITIVE 1 (BRI1).
BES1 (BRI1-EMS SUPRESSOR 1): transcription factor responsible for BR-
regulated gene expression.
bes1-D (BES1 dominant): mutant with enhanced BES1 signaling.
BIK1 (BOTRYTIS-INDUCED KINASE1): the membrane-anchored BIK1 plays
distinct roles in Arabidopsis resistance to necrotrophic and biotrophic
pathogens.
BIM1 (BES1-INTERACTING MYC-LIKE 1): basic helix–loop–helix (bHLH) tran-
scription factor involved in BR signaling and embryonic patterning in
Arabidopsis.
BIN2 (BRASSINOSTEROID INSENSITIVE 2): a glycogen synthase kinase with
negative regulation in BR signaling.
BKI1 (BRI1 KINASE INHIBITOR 1): inhibits heterodimerization of BRI1 with
BAK1.
BL (Brassinolide): a highly active form of BR.
BR6OX (BRASSINOSTEROID-6-OXIDASE): such as CYP85A1 and CYP85A2
implicated in BR biosynthesis.
BRI1 (BRASSINOSTEROID INSENSITIVE 1): a leucine-rich repeat receptor-like
kinase that perceives the BR signal.
BRX (BREVIS RADIX): root meristem growth regulator, an auxin-responsive
gene.
Brz (Brassinazole): a BR biosynthesis inhibitor.
BSK1 (BR-SIGNALING KINASE 1): a member of the BSK family that activates
BR signaling downstream of BRI1.
BSU1 (BRI1 SUPPRESSOR 1): a phosphatase involved in BR signaling.
BU1 (BRASSINOSTEROID UPREGULATED 1): encoding a bHLH protein that is
involved in BR signaling and controls bending of the lamina joint in rice.
BZR1 (BRASSINAZOLE RESISTANT 1): a master regulator controlling BR-
related gene expression.
bzr1-D (BZR1 dominant): mutant with enhanced BZR1 signaling.
CDG1 (CONSTITUTIVE DIFFERENTIAL GROWTH 1): a receptor-like cytoplasmic
kinase implicated in the inactivation of BIN2 through dephosphorylation.
CESTA: a bHLH transcription factor positively regulating BR biosynthesis.
ChIP (chromatin immunoprecipitation): method used to investigate the
interactions between proteins and DNA in the cell.
CKX3 (CYTOKININ DEHYDROGENASE/OXIDASE 3): CKX3 catalyzes the
degradation of cytokinins.
COI1 (CORONATINE INSENSITIVE1): an F-box protein required for jasmonic
acid responses.
COR15A (COLD-REGULATED 15A): cold-responsive gene in Arabidopsis.
CPD (CONSTITUTIVE PHOTOMORPHOGENESIS AND DWARFISM): a hydro-
xylase involved in BR biosynthesis.
cps1-1: mutant of ent-copalyl diphosphate synthase, a gibberellin (GA)
metabolic enzyme.
d35: mutant of ent-kaurene oxidase enzyme involved in early step of GA
biosynthesis.
DELLA proteins: negative regulators of GA signaling, containing the DELLA
motif of 17 amino acids in their N-terminal region.
DET2 (DE-ETIOLATED 2): a key enzyme of the BR biosynthetic pathway.
DWF1 (DWARF1): catalyzes the rate-determining step in BR biosynthesis.
DWF4 (DWARF4): catalyzes the rate-determining step in BR biosynthesis.
DWF5 (DWARF5): encodes a putative sterol delta-7 reductase involved in BR
biosynthesis.
EBR (24-epibrassinolide): a biologically active type of BR.
Eix (Ethylene-inducing xylanase): Eix serves as receptor for the fungal elicitor.
ELF6 (EARLY FLOWERING 6): involved in flowering time in Arabidopsis.
EMS (ETHYL METHANESULFONATE): a compound that is often used in
mutagenesis.
ERD10 (EARLY RESPONSIVE TO DEHYDRATION 10): implicated in stress
tolerance and induced by water stress, ABA and cold stress.
EXP (EXPANSIN): cell wall-loosening protein.
FCA (FLOWERING CONTROL LOCUS A): a flowering time control gene in
Arabidopsis that encodes a protein containing RNA-binding domain.
2
Trends in Plant Science xxx xxxx, Vol. xxx, No. x
FER (FERONIA): receptor-like kinase mediating male–female interactions
during pollen tube reception.
FLC (FLOWERING LOCUS C): a MADS [MCM1, AGAMOUS, DEFICIENS and SRF
(serum response factor)] domain transcription factor that acts as a repressor of
flowering.
flg22 (FLAGELLIN 22): a microbial-associated molecular pattern.
FLS2 (FLG-SENSING 2): a binding receptor for flg22.
GA20x (Gibberellin 20-oxidase): implicated in feedback regulation of GA
biosynthesis.
GASTs (Gibberellin-stimulated transcripts): genes whose expression is
stimulated by GAs.
GATA: GATA-binding transcription factors that contain either one or two highly
conserved zinc-finger DNA-binding domains.
GhGAI1 (Gossypium hirsutum gibberellic acid-insensitive 1): gene encoding a
DELLA-type repressor of GA signaling in cotton.
GUS: a b-glucuronidase-encoding gene that is usually used to make
promoter:GUS fusion constructs for histochemical assays.
IPT (ISOPENTYL TRANSFERASE): catalyzes the rate-limiting step of isoprenoid
cytokinin biosynthesis.
LD (LUMINIDEPENDENS): a gene involved in the control of flowering time in
Arabidopsis.
MAMP (MICROBIAL ASSOCIATED MOLECULAR PATTERNS): highly conserved
molecular signatures that are recognized by cells of the innate immune
system.
MAPK (MITOGEN-ACTIVATED PROTEIN KINASE): implicated in the broad
regulation of multiple physiological and defense responses in plants.
NaJAR4 (Nicotiana attenuta JASMONATE RESISTANT4): enzyme catalyzing
the joining of isoleucine (Ile) to JA to form JA-Ile.
NaJAR6 (Nicotiana attenuta JASMONATE RESISTANT6): enzyme catalyzing
the joining of isoleucine (Ile) to JA to form JA-Ile.
NaTD (Nicotiana attenuta threonine deaminase): NaTD catalyzes the conver-
sion of threonine to isoleucine in N. attenuata.
NPR1 (NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1): a master
regulatory protein of plant disease resistance.
OsGSK1 (Oryza sativa GLYCOGEN SYNTHASE KINSASE1): a rice ortholog of
Arabidopsis BIN2.
OsGSR1 (Oryza sativa GAST family gene in rice 1): a member of GAST family
in rice.
OsNPR1 (Oryza sativa NONEXPRESSOR OF PATHOGENESIS-RELATED
GENES1): a master regulatory protein of plant disease resistance.
OsSLR1 (Oryza sativa Slender Rice 1): a repressor of GA signaling in rice.
OsWRKY45 (Orzya sativa WRKY): a WRKY transcription factor playing a crucial
role in benzothiadiazole-induced blast resistance in rice.
PCF: promoter-linked coupling element-binding factor.
PIN (PIN-FORMED): a group of transmembrane proteins with a predicted
function of secondary transporters and a rate-limiting role in the catalysis of
auxin efflux from cells.
PP2A (Protein Phosphatase 2A): a phosphatase involved in regulation of BR
signaling.
psc1 ( partially suppressing coi1): partial suppressor mutant of coil1.
PYK10 (PHOSPHATE STARVATION-RESPONSE 3.1): encodes a hydrolase that
hydrolyzes O-glycosyl compounds in Arabidopsis.
RD22 (RESPONSIVE TO DESSICATION 22): gene implicated in stress tolerance
and induced by water stress, ABA and salt stress.
RD29A (RESPONSIVE TO DESSICATION 29A): gene implicated in stress
tolerance and induced by water stress, ABA, cold and salt stresses.
REF6 (RELATIVE OF EARLY FLOWERING 6): a repressor of FLC that is involved
in histone demethylation and deacetylation.
RNAi (ribonucleic acid interference): a technology used to repress the activity
of given gene(s) in the cell.
ROP (RHO OF PLANTS): Rho family GTPases implicated in auxin transport.
ROT3 (ROTUNDIFOLIA 3): a BR biosynthetic pathway enzyme.
sax1 (HYPERSENSITIVE TO ABSCISIC ACID AND AUXIN): a BR biosynthetic
mutant with hypersensitivity to ABA and auxin.
SBI1 (SUPPRESSOR OF BRI1): a leucine carboxyl methyltransferase involved in
methylation of PP2A to deactivate BRI1.
SDG (SET domain-containing group): SDG genes encode H3K36 methyltrans-
ferases, which regulate the methylation of histone lysine residues in plants.
SERK family: somatic embryogenesis receptor kinase family to which the
BAK1/SERK3 and its homologs (SERK1, SERK2 and SERK4) belong.
SET [Su(var)3-9/E(z)/Trithorax]: SET domain is a conserved amino acid motif
of proteins that are implicated in the epigenetic control of gene expression.
SPCH (SPEECHLESS): a basic helix–loop–helix (bHLH) stomatal initiating
factor.
TCP1 [TEOSINTE BRANCHED 1, CYCLOIDEA and PCF1 (promoter-linked
coupling element-binding factor)]: TCP1 is a TCP domain-containing transcrip-
tion factor involved in the regulation of DWF4 expression.
Waito-C (GA biosynthetic mutant): mutant of GA biosynthetic 3b-hydroxylase
enzyme.
YDA: also known as YODA, a MAPK Kinase Kinase (MAPKK) negatively
regulating stomatal development.
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Review Trends in Plant Science xxx xxxx, Vol. xxx, No. x

BR homeostasis BR biosynthesis
BR biosynthesis

Active BL Active 24- BZR1 TCP1 Aux CESTA

26 Active BL and CS
and CS epiBR C-
at

Gl at C C5
and CS prec BL
n

yc
Com
tio 1

os 23
Sulfate

UC T73
yla

BEN1,
AtST4a 4A

UG
AtST1

yla
x 3

T7 C6
addition BRX o

pe
dr P7

-
ti o
3
Hy CY

tit

n
io
C
Inactive BL and CS or

n
Y
ursors

P
to
24-epiBR Inactive BL and Inactive BL and

72C1
CS CS

BR homeostasis
BR homeostasis

OH
OH
ROT3
CYP90D1 OH DE OH
T2
DE

T3 1 OH
OH RO 90D OH BR biosynthesis
T2

22-HCR P 22-dHCR
Y
OH C O H 22-d-dTE
OH CY
CY P85
ROT3 P8 A1
CYP90D 5A
O 1 2
H
22-H-ergostan- OH H 3-epi-6dCT
3-one OH OH
OH
4

OH OH
DWF

OH
DWF4 CPD OH OH OH
HO
ROT3
HO O HO dTY HO H
H HO H dCT HO H dDT H dCS
H dTE OH
CN
T2
DE

CYP85A1 OH
CYP85A1 CYP85A1 CYP85A2 HO
DWF4
CYP85A2 CYP85A2
HO O
HO BL
CR 2
HO 5A
OH OH P8
OH OH OH CY
CPD
OH
ROT3 OH OH OH
HO
HO HO HO HO
HO H O H O HO HO
O H H
6-oxo-CN CT TE O DT O TY CS

TRENDS in Plant Science

Figure 1. Proposed model for brassinosteroid (BR) biosynthesis and BR homeostasis in Arabidopsis. BR biosynthesis: DET2 (DE-ETIOLATED 2) catalyzes the conversion of
campesterol (CR, precursor of BRs) to campestanol (CN); DWF4 (DWARF4) catalyzes the conversion of CN to 6-oxocampestanol (6-Oxo-CN); DWF4 brings conversion of CN
and 6-Oxo-CN to 6-deoxocathasterone (dCT) and cathasterone (CT); CPD (CONSTITUTIVE PHOTOMORPHOGENESIS AND DWARFISM) and ROT3 (ROTUNDIFOLIA 3)
catalyze the formation of 6-deoxoteasterone (dTE) and teasterone (TE) from dCT and CT, respectively; CYP85A1 and CYP85A2 catalyze the formation of 3-dehydro-6-
deoxoteasterone (dDT), 3-dehydroteasterone (DT), 6-deoxotyphasterol (dTY), typhasterol (TY), 6-deoxocastasterone (dCS) and castasterone (CS) in three independent
steps; CYP85A2 catalyzes the formation of brassinolide (BL, an active BR) from CS; DWF4 also catalyzes the conversion of CR to 22-hydroxycampesterol (22-HCR); ROT3 and
CYP90D1 bring the conversion of 22-HCR to 22,23-dihydroxycampesterol (22-dHCR); DET2 catalyzes the formation of (22S, 24R)-22-hydroxy-ergostan-3-one (22-H-ergostan-
3-one) and 3-dehydro-6-deoxoteasterone (22-d-dTE) from 22-HCR and 22-dHCR; 22-H-ergostan-3-one isomerizes to 3-epi-6-deoxocathasterone (3-epi-6dCT); ROT3 and
CYP90D1 catalyze the formation of dTY from 3-epi-6dCT; CYP85A1 and CYP85A2 catalyze the formation of dDT from 22-d-dTE. In BR homeostasis, the strong repression of
CPD and DWF4 genes encoding key BR biosynthetic enzymes by BZR1 (BRASSINAZOLE RESISTANT 1) represents an intrinsic BR homeostatic control. DWF4 is under
positive regulation of the TCP1 (TEOSINTE BRANCHED 1, CYCLOIDEA and PCF1). Auxin (Aux)-induced transport of BRX (BREVIS RADIX) to the nucleus also promotes CPD
and DWF4 expression in Arabidopsis roots. CESTA positively regulates BR biosynthesis by stimulating the expression of CPD. BR homeostasis is also maintained through
inactivation of active brassinolide (BL) and CS by hydroxylation at the C-26 position by CYP734A1. Glycosylation at C-23 by uridine diphosphate (UDP)-glycosyltransferases
(UGTs), namely UGT73C5 and UGT73C6, also renders BRs inactive. CYP72C1 binding to BL precursors inactivates the BL precursors to maintain BR homeostasis. The bri1-5
ENHANCED 1 (BEN1) encoding a protein homologous to dihydroflavonol 4-reductase and anthocyanidin reductase regulates BR homeostasis by reducing the synthesis of
active BRs by competing with BL and CS precursors for the active site on BR biosynthesis enzymes. Sulfonation of BL, CS and 24-epibrassinosteroids (24-epiBR) by
Arabidopsis sulfotransferases (AtST), namely AtST4a and AtST1, also renders BRs nonfunctional.

LRR21 induces partial BRI1 kinase activity that phos- subsequently activate the BSU1 phosphatase, which in
phorylates BKI1 on Tyr211, resulting in its dissociation turn inactivates BIN2 through dephosphorylation
from the membrane. The removal of BKI1 initiates the [1,39,40]. Dephosphorylation relieves BIN2 suppression
association and sequential transphosphorylation of on BZR1 and BES1. This results in the accumulation of
BRI1with BAK1 [34]. Moreover, detached BKI1 can dephosphorylated BZR1 and BES1, which move to the
enhance BR signaling by antagonizing 14-3-3 proteins. nucleus to regulate BR-related gene expression directly
The 14-3-3 proteins are involved in the binding and or via an interaction with other TFs, such as AtIWS, BIM
cytoplasmic retention of BZR1 and BES1 (also named and GATA-binding TFs [6,41–44]. A recent study has
as BZR2), the two master TFs of BR signaling [33,35–38]. indicated that SBI1 and PP2A are also involved in BR
Activated BRI1 phosphorylates BR signaling kinases signaling. Specifically, methylated PP2A dephosphory-
(BSKs) at Ser230 and the CDG1 at Ser234, which lates BRI1, whereas BR-induced SBI1 methylates PP2A
3
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Review Trends in Plant Science xxx xxxx, Vol. xxx, No. x

BRI1 BRI1
– BRs + BRs
BRI1:BAK1
BAK1 heterodimer

BR
BAK1 BR-binding site

SBI1 SBI1
BSK1 CDG1
B
BSK1 CDG1
CD
BKI1
1 CH 3 P P
PP2A
P P P P PP2A
BSU1
BSU1
1 P
P B
BKI1
PB
BIN2 BRI1 endocytosis

BIN2 P BIN2
B
Proteasomal degradation P
-3
-3

P
14

BZR1/BES1
B
P P P P PP2A BZR1/BES1
B

P B
BIN2 Other TFs
P P
BZR1/BES1
BZR1/BES1
S1 P P BZR1/BES1

Nucleus
BR-target genes
Cytosol

BR-induced regulation of target genes

TRENDS in Plant Science

Figure 2. Current model of brassinosteroid (BR) signaling in the presence and absence of BRs in Arabidopsis. In the absence of BRs, BRI1 (BRASSINOSTEROID
INSENSITIVE 1), a BR receptor kinase, remains inactive and does not heterodimerize with BAK1 (BRI1-ASSOCIATED RECEPTOR KINASE 1), its coreceptor. BIN2
(BRASSINOSTEROID INSENSITIVE 2), a negative regulator of BR signaling, constitutively phosphorylates BZR1 (BRASSINAZOLE RESISTANT 1) and BES1 (BRI1-EMS
SUPRESSOR 1), the two master transcription factors (TFs) of BR-induced responses. Phosphorylation of BZR1 and BES1 by BIN2 attracts the binding of 14-3-3 proteins. This
in turn promotes the cytoplasmic retention of the TFs, rendering them unable to enter the nucleus and terminates the BR-induced response. In the presence of BRs, the
binding of BRs to BRI1 initiates autophosphorylation to induce partial BRI1 kinase activity. This results in the dissociation of BRI1 kinase inhibitor BKI1 (attached at the BRI1
kinase domain), followed by the heterodimerization of BRI1 with BAK1 and transphosphorylation to impart full BRI1 kinase activity. Fully activated BRI1 then phosphorylates
BR-SIGNALING KINASES (BSKs) and CDG1 (CONSTITUTIVE DIFFERENTIAL GROWTH 1). Subsequently, activated BSKs and CDG1 phosphorylate BSU1 (BRI1
SUPPRESSOR 1), which finally dephosphorylates BIN2. This in turn relieves the suppression of BIN2 on BZR1 and BES1, leading to the accumulation of dephosphorylated
BZR1 and BES1. Dephosphorylated BZR1 and BES1 enter the nucleus and function to regulate the expression of BR target genes, either through direct interaction or via an
interaction with other TFs. PP2A (Protein Phosphatase 2A) also positively regulates BR signaling by dephosphorylating BZR1 and BES1, whereas the SBI1 (SUPPRESSOR OF
BRI1) is involved in the deactivation of BRI1 through methylation of PP2A.

and controls its membrane-associated subcellular locali-
zation [45,46].
BR homeostasis and plant growth
As indicated by stunted root and shoot growth of BR
biosynthetic mutants (dwf7-1, det2, cpd, br6ox, rot3) or
abnormal shoot and root growth patterns of BR signaling
mutants (bri1, bak1, bzr1-D, bes1-D), BR homeostasis at
endogenous BR levels and at BR signaling levels is vital for
normal biological processes [1,2,25,47]. For instance, anal-
yses of loss-of-function bri1-116 and gain-of-function bes1-
D mutants indicated that a balance in BR signaling is
required to maintain optimal meristem size and overall
root growth. The bri1-116 mutant has reduced root meri-
stem size, which is linked with decreased mitotic activity
and low activity in the quiescent center. Interestingly, in
BR-treated plants and in the bes1-D mutant, which has
enhanced BR signaling, reduced root meristem sizes were
4
attributed to the premature cell cycle exit, which resulted
in the early differentiation of meristematic cells [4]. Re-
duced BR titers (det2-1 mutation) or perturbed BR signal-
ing (bri1-301 mutation) also have adverse impacts on
cellulose biosynthesis, which contributes to cell wall for-
mation during cell expansion and elongation [48].
BR homeostasis is primarily achieved through tight
feedback regulation of BR metabolic genes by BR signaling
elements, with strong repression of transcription following
BR application and significant upregulation in response to
inhibition of BR biosynthesis. Furthermore, the inactiva-
tion of bioactive BRs through hydroxylation, glycosylation
and sulfonation constitutes vital components that control
BR homeostasis [49–51] (Figure 1).
BR signaling in plant growth and immunity
Over the past several years, intensive research efforts have
elucidated the roles of BR signaling elements regarding
TRPLSC-983; No. of Pages 12
Review
overall plant growth, development and immunity. Here,
we discuss the most recent findings that have emerged
from this research area.
Vegetative growth
Previous expression studies have demonstrated that BRs
regulate the expression of cell expansion genes. Expansins
(EXPs) induce cell wall extension for the growth of plant
cells. A recent study demonstrated that BRs are involved in
the regulation of EXP levels in Arabidopsis. When treated
with exogenous BRs, the expression of an AtEXP gene
(AtEXPA5) was downregulated in det-2 and bri1-301
mutants but upregulated in the dominant bzr1-D mutant
and in wild-type (WT) plants. Furthermore, the bzr1-1
DXexpA5-1 double mutant showed reduced growth com-
pared with the bzr1-D single mutant. Taken together,
these data provide evidence for the regulation of AtEXPA5
by BR signaling downstream of BZR1 [52].
Methylation of histone lysine residues is implicated in
epigenetic regulation of gene expression in plants. In rice
(Oryza sativa), it was recently reported that a H3K36
methyltransferase encoded by SDG725 is crucial in the
methylation of histone lysine residues. Downregulation of
SDG725 was associated with dwarfism, shortened inter-
nodes, erect leaves and small seeds; features that are
typical of BR mutants. Deletion of SDG725 resulted in
more than a twofold downregulation of several key BR-
related genes, such as OsDWARF11, BRI1 and BU1. In
addition, ChIP (chromatin immunoprecipitation) data
showed a reduced level of H3K36me2 and H3K36me3 in
chromatin at several regions of the examined 30 -coding
regions of these BR-related genes in SDG725 knockdown
plants. Moreover, the SDG725 protein was able to bind
directly to the BR target genes. These results demonstrate
the role of SDG725-mediated H3K36 methylation in mod-
ulating the expression of BR target genes, which is crucial
for regulating the growth and development of rice [53].
Reproductive growth
Floral development is an important transition from the
vegetative phase and is regulated by several endogenous
and environmental signals [54,55]. BR signaling promotes
flowering by enhancing the expression level of LD and FCA
autonomous pathway genes, which in turn suppress the
FLC gene [54,56]. BR induction of the floral pathway
independent of LD and FCA has also been suggested in
Arabidopsis. Studies conducted in bri1 mutants exhibiting
a weak late flower phenotype and partial sensitivity to
vernalization did not show altered expression of LD and
FCA genes. These data support the existence of a LD- and
FCA-independent pathway of floral induction that is me-
diated by BR-induced suppression of FLC [56,57]. In addi-
tion, BES1 was shown to regulate the expression of ELF6
and REF6 genes, which are involved in the control of
flowering time. Specifically, ELF6 functions in the photo-
periodic flowering pathway and REF6 acts as a repressor of
FLC [58].
Stomatal development
Although BRs inhibit chloroplast development in Arabi-
dopsis [59], the direct functional role of BRs in stomatal
Trends in Plant Science xxx xxxx, Vol. xxx, No. x
development is not entirely understood. Recently, BRs
have been shown to play a crucial regulatory role in
stomatal development by activating the MAPK kinase
kinase (MAPKKK) YDA [13], which has been implicated
as a negative regulator of stomatal development in Arabi-
dopsis [60,61]. In the absence of BRs, BIN2 represses YDA
function through phosphorylation, leading to a reduction in
MAPK pathway activity. This in turn leads to the dere-
pression of SPCH (SPEECHLESS), allowing SPCH to
initiate stomatal development. In the presence of BRs,
BR signaling activates the MAPK pathway by inactivation
of BIN2 through BRI1, BSK1 and BSU1, resulting in the
inhibition of stomatal production [13].
Contrary to the aforementioned report [13], a recent
study in Arabidopsis shows positive implication of BRs in
stomatal development by inhibition of BIN2-mediated
phosphorylation of SPCH [62]. In the absence of BRs, in
addition to MAPK, BIN2 also phosphorylates residues
overlapping the MAPK target domain and four residues
located in the amino-terminal region outside of the MAPK
target domain of SPCH. These phosphorylation events of
SPCH by BIN2 inhibit SPCH activity and limit epidermal
cell proliferation. Conversely, the presence of BRs inhibits
BIN2 activity, thereby stabilizing SPCH that initiates
excessive stomatal and non-stomatal cell formation [62].
Innate immunity
The triggering of innate immunity is a costly tradeoff
between growth and immunity in plants and animals
[14,63–65]. Although it is known that BRs induce disease
resistance in rice and tobacco (Nicotiana tabacum) [66], the
molecular mechanisms underlying this functional role
have remained elusive. Intensive studies have deciphered
complex positive and negative roles of BRs and BR signal-
ings in innate immunity that involve crucial functions of
BRI1 and BAK1 [14,31,67,68].
Among the pathogen- or microbial-associated molecu-
lar patterns (PAMP or MAMPs), flagellin 22 (flg22) and
chitin are well characterized. The binding of flg22 to its
receptor flg-sensing 2 (FLS2) initiates metabolic activities
to arrest pathogen proliferation [67–69]. Similar to the
BR-induced BRI1 signaling, the binding of flg22 to FLS2
triggers an association and transphosphorylation with
BAK1, thereby activating FLS2. The activated FLS2 sub-
sequently phosphorylates BIK1 to transduce the target
response [67,70,71]. The function of BAK1 as a coreceptor
of BR-induced BRI1 signaling and flg22-induced FLS2
signaling indicates the potential tradeoff between BR
and FLS2 signalings through the mediation of BAK1.
However, a recent study has suggested the existence of
BAK1-independent immune signaling. In plants treated
with both BRs and flg22, BRs were found to significantly
decrease flg22-induced MAMP-triggered immunity (MTI)
responses. By contrast, treatment with flg22 had no
effect on BR-induced responses. When BRs and flg22 were
applied to plants separately, they induced distinct gene
expression profiles and biochemical responses. Collective-
ly, these data suggest a unidirectional inhibition of FLS2-
mediated immune signaling by BR perception that occurs
independently of complex formation with BAK1 and asso-
ciated downstream phosphorylation [11]. Consistent with
5
TRPLSC-983; No. of Pages 12

Review Trends in Plant Science xxx xxxx, Vol. xxx, No. x

(a)
ing flg22
ing
flg22
nd nd BR
Bi BRI1 Bi din
g
FLS2 BRI1 Bin
FLS2 Association and
Transphosphorylation
Association + BRs
– BRs

BSK BSK
BAK1 CDG BIK1 BAK1 CDG
BAK1 BAK1
BIK1 Inactive BSU
BSUs BAK1
Innate immunity

BIN2 Active BSUs

ism
Unknown mechan anism BIN2
BZR1 n mech
Unknow BZR1
BES1
ism MAPK
MAPK Unknown mechan n mech
anism BES1
Unknow
No BR-induced Reduced BR-induced
Immunity Cytosol responses immunity responses

(b) Abiotic stress tolerance Abiotic or biotic stress tolerance BRs

BRs

Active BR signaling
NO NADPH
oxidase
Abiotic ABA H2O2 BZR1 and BES1
stress
ROS
Upregulated an Nucleus
tioxidant system
,
Abiotic stress

PCs, GSH, AS
Damage to nucleic A, proline etc.
response

acids, proteins and

BR-regulated gene expression
membrane
Cytosol

Reduced cell Improved cell

viability viability
TRENDS in Plant Science

Figure 3. Current model of brassinosteroids (BRs) implicated in innate immunity and abiotic stress responses in Arabidopsis. (a) In the absence of BRs, flg22 (FLAGELLIN
22) binds to FLS2 (FLG-SENSING 2), a receptor of flg22, and initiates the association and transphosphorylation between BAK1 (BRI1-ASSOCIATED RECEPTOR KINASE 1)
and FLS2. Activated FLS2 phosphorylates the downstream receptor-like cytoplasmic kinase BIK1 (BOTRYTIS-INDUCED KINASE1) to trigger innate immunity via a MAPK
(MITOGEN-ACTIVATED PROTEIN KINASE) pathway. In the presence of BRs, the FLS2-mediated signaling pathway is suppressed through BRI1 (BRASSINOSTEROID
INSENSITIVE 1) in a BAK1-dependent or -independent manner, depending upon endogenous BR and BRI1 levels. Other BR signaling components, such as BIN2
(BRASSINOSTEROID INSENSITIVE 2), BZR1 (BRASSINAZOLE RESISTANT 1) and BES1 (BRI1-EMS SUPRESSOR 1), might also be involved in the suppression of FLS2
signaling downstream of BIK1, perhaps independently of BAK1, by an unknown mechanism. (b) Abiotic stress leads to the production of reactive oxygen species (ROS),
which damage nucleic acids, proteins and cell membranes, resulting in reduced cell viability. Active BR signaling regulates the expression of BR target genes that are
involved in the induction of antioxidant systems and metabolites that render protection to nucleic acids, proteins and cell membranes. As a result of this induced
antioxidant activity and cell viability, the overall stress tolerance is improved through this beneficial activity imparted by BR function. Active BR signaling can induce gene
expression of the nicotinamide adenine dinucleotide phosphate (NADPH) oxidase to regulate H2O2 production to confer abiotic and biotic stress tolerance. Active BR
signaling can also upregulate nitric oxide (NO) production, which promotes abscisic acid (ABA) biosynthesis, resulting in stress tolerance. Abbreviations: ASA, ascorbic
acid; GSH, glutathione; PCs phytochelatins.

all of the aforementioned observations, another indepen- many genes that govern several biological processes, such
dent study has provided evidence that implicates BRs in as seed germination, stomatal closure and responses to
MTI responses in both BAK1-dependent and -independent environmental stresses [74–77]. Analyses of the BR-relat-
pathways. The association of BRs with MTI responses was ed mutants (det2-1 and bri1-1) have demonstrated that
dependent upon endogenous BR and BRI1 levels [12] they show increased sensitivity to the inhibitory effects of
(Figure 3a). ABA during seed germination in comparison with WT [74].
However, primary root and hypocotyl elongation assays in
Interactions and crosstalk between BRs and other the sax1 mutant revealed hypersensitive responses to
hormones in plant growth and stress responses ABA, as well as Aux and ET [78]. Both BRs and ABA exert
BRs and ABA a promoting effect on stomatal closure which is most likely
ABA regulates both stress- and nonstress-related plant mediated via nitric oxide (NO) functioning as a mediator of
responses by acting as a signal molecule [72,73]. Interac- ABA-induced stomatal closure in plants. This hypothesis is
tions between BRs and ABA regulate the expression of supported by the observation that NO was shown to
6
TRPLSC-983; No. of Pages 12
Review
mediate both ABA-induced stomatal closure and BR-in-
duced ABA biosynthesis [75,79,80]. In addition, the coap-
plication of BRs and ABA has been reported to result in a
synergistic increase in drought-protective effects that were
greater than those observed with either ABA or BR treat-
ments alone [81]. Furthermore, Arabidopsis and Brassica
napus seedlings treated with BRs showed enhanced toler-
ance to drought and cold stresses, which was accompanied
by the induction of ABA- and multiple stress-inducible
RD29A, ERD10 and RD22 genes [76]. Moreover, microarray
analyses have shown that a large proportion of BR-respon-
sive genes are also regulated by ABA [82]. An additional
independent study provided further evidence demonstrat-
ing that the exogenous application of BRs enhances water
stress tolerance by increasing ABA biosynthesis via the
mediation of BR treatment-induced NO production [80].
Recently, it was proposed that the signaling cascades of
ABA and BRs crosstalk just after the perception of BRs and
before their transcriptional activation [5]. Analysis of the
BR signaling mutant bri1-116 and subcellular localization
of BKI1 revealed that the BR–receptor complex was not
required by ABA to act on BR signaling outputs. However,
ABA action in BR signaling was dependent on BIN2 be-
cause application of ABA was unable to inhibit BR signal-
ing outputs when BIN2 was inhibited by application of
LiCl, a BIN2 inhibitor. Furthermore, studies on ABA
insensitive abi1 and abi2 mutants indicated that ABA
was unable to act on BR signaling outputs in these
mutants, suggesting that early ABA signaling components
(ABI1 and ABI2) are implicated in ABA regulation of BR
signaling outputs [5].
BRs and Aux
The synergistic interactions of BRs and Aux play promi-
nent roles in several aspects of plant growth and develop-
ment [30]. The direct interaction between BIN2 and ARF2
represents an example of the synergistic effects of BRs and
Aux in photomorphogenesis. Phosphorylation of ARF2 by
BIN2 results in a loss of the DNA-binding repression
activities of ARF2, indicating that BIN2 is capable of
regulating the expression of Aux-induced genes through
direct inactivation of ARF repressors, leading to the syn-
ergistic effect of BRs and Aux [83]. In addition, the appli-
cation of BRs enhances polar Aux transport and
endogenous Aux distribution by upregulating the expres-
sion of PIN and ROP genes, which are functionally in-
volved in the distribution of Aux [84]. Furthermore, high
levels of BRI1 expression in the epidermis results in an
enlarged root meristem, whereas reduced BRI1 expression
accounts for the small root meristem size in the bri1
mutant. The activity of BRs in the meristem was later
shown to be accompanied by transcriptional modulation
and post-transcriptional regulation of PIN2 and PIN4
genes [8,85]. The influence of BRs on PIN Aux efflux
carriers, which control mitotic activity and cell differenti-
ation, suggests a possible mechanism that contributes to
BR-mediated root growth through regulation of Aux
distribution.
The specific signals that initiate BR biosynthesis are
largely unknown. In a recent study, Aux was shown to
function as a biosynthesis signal for BRs in Arabidopsis [9].
Trends in Plant Science xxx xxxx, Vol. xxx, No. x
Exogenous applications of Aux to DWF4pro:GUS plants
were shown to enhance DWF4 expression and concomi-
tantly increase endogenous BR levels. Analysis of the
DWF4pro:GUS construct in BR- and Aux-mutant back-
grounds indicated that Aux-induced expression of DWF4
occurs independently of BRs and only requires the Aux-
signaling pathway. These data suggest that Aux exerts a
direct control on BR biosynthesis in plants. In addition,
Aux was shown to directly control BR signaling by inhibit-
ing the binding of the BZR1 repressor to the DWF4 pro-
moter. However, disruption in BR biosynthesis has been
shown to have an adverse impact on Aux-responsive genes,
which is consistent with previous findings [83].
BRs and ET
ET biosynthesis is regulated by a large number of extrinsic
and intrinsic cues [86]. The ACSs are rate-limiting factors
of ET biosynthesis [87]. BRs positively influence ET bio-
synthesis through regulation of ACS and ACC oxidase
activities [88]. Recently, BRs have been shown to be
involved in ET-induced growth responses through FER.
The FER gene encodes a RLK that is implicated in pollen
tube perception and cell elongation and is required for a
normal ET response. The etiolated fer-2 mutant exhibited
hypersensitivity to ET but partial insensitivity to BRs.
Moreover, BRs were unable to antagonize the ET effects
on hypocotyl growth in the fer-2 mutant, indicating
FER-dependent BR effects on ET-induced growth
responses [89,90]. There is also an increasing amount of
evidence suggesting interactions between BRs and ET in
defense responses. Eix proteins are strong elicitors of plant
defense responses in several cultivars. For instance, two
Eix RLK receptors of tomato (Solanum lycopersicum
LeEix1 and LeEix2) both bind to Eix. However, only
LeEix2 is actually involved in mediating defense
responses, whereas LeEix1 heterodimerizes with LeEix2
and attenuates the signaling of LeEix2. Furthermore, the
attenuating function of LeEix1 requires the binding of
LeEix1 to BAK1, providing evidence for the interaction
between BRs and ET in responses to Eix [7].
BRs and CKs
The roles of CKs in plant development and responses to
various stresses have been widely characterized [91–96].
Recently, several lines of evidence have suggested the
existence of interactions and crosstalk between BRs and
CKs in various biological processes. Overexpression of the
CKX3 gene with the root-specific promoter PYK10 resulted
in a reduction of CK levels in Arabidopsis roots, leading to
enhanced root growth and slightly reduced leaf growth
[92]. Overexpression of BRI1 in PYK10:CKX3 plants using
its own promoter further enhanced root growth and
resulted in leaf growth similar to WT levels. These findings
are in agreement with those observed when PYK10:CKX3
plants were treated with BRs, suggesting that crosstalk
between BRs and CKs is involved in the regulation of plant
growth [10]. In addition, overexpression of an IPT gene,
which results in an increase in CK content, also provides
possible links between CK and BR signaling pathways [97].
An increase in CK content just before the onset of senes-
cence by the conditional overexpression of IPT in rice
7
TRPLSC-983; No. of Pages 12
Review
results in enhanced tolerance to drought stress. The ob-
served increase of CKs coincided with the upregulation of
several BR-related genes, such as BAK1, BSK1, SERK1
and DWF5, suggesting that crosstalk between BRs and
CKs may contribute to the modification of source–sink
relations, leading to increased drought tolerance [97].
BRs and JA
The interaction of BRs and JA plays crucial roles in plant
development and stress responses [98–100]. The COI1 is
an F-box protein that is required for the execution of JA
signaling and JA responses in Arabidopsis [101]. The psc1
mutant with partial suppression of coi1insensitivity to JA-
induced inhibition of root growth is a leaky mutation of
DWF4 [98]. Application of BRs was able to eliminate
partial restoration of JA sensitivity of the psc1 mutant
in coi1-2 and JA hypersensitivity of psc1 in WT. Further-
more, expression analysis indicated that DWF4 expression
was repressed by JA in a COI1-dependent manner. These
results demonstrated that BRs negatively regulate JA-
induced inhibition of root growth. Secondly, these data
confirm that JA-induced downregulation of DWF4 occurs
downstream of COI1 in the JA signaling pathway [98].
Recently, BAK1 was shown to confer resistance to Nico-
tiana attenuata against its specialist herbivore, Manduca
sexta [100]. Altered expression of NaBAK1 was observed in
plants exposed to larval oral secretions (LOS) of M. sexta.
NaBAK1-silenced plants, when wounded or applied with
LOS, exhibited attenuated JA and JA–isoleucine bursts
independently of compromised MAPK activity or elevated
SA levels. JA application to the NaBAK1-silenced plants
induced higher levels of defensive trypsin proteinase inhi-
bitors. In addition, transcription of NaTD was reduced,
whereas NaJAR4 and NaJAR6 expression was increased
in the NaBAK1-silenced plants. These data demonstrate
that BAK1 plays an essential role in mediating the resis-
tance of N. attenuata to M. sexta by modulating herbivory-
induced JA accumulation and controlling the activity of
defensive secondary metabolites [100].
BRs and SA
Increasing evidence suggests that crosstalk between BRs
and SA plays an important role in plant response to biotic
and abiotic stresses. As a challenge to the prevailing view
that BRs positively regulate innate immunity [66], a recent
study showed that BR-induced modulation of immunity
responses, partly through the negative crosstalk between
BRs with SA, could enhance the susceptibility of rice to the
root oomycete Pythium graminicola [102]. Rice seedlings
treated with BRs showed increased susceptibility towards
P. graminicola. Application of Brz, a BR biosynthesis
inhibitor, to rice plants, consistently revealed reduced
susceptibility against P. graminicola. This was shown to
be the result of the repression of SA defense responses by
BRs downstream of SA biosynthesis but upstream of key
defense regulators, namely OsNPR1 and OsWRKY45.
These data support the hypothesis that P. graminicola
exploits the BR pathway as a decoy to counteract the
effective SA-induced defense responses in rice. This report
clearly highlights the implication of BRs as a negative
regulator of immunity against pathogens and also
8
Trends in Plant Science xxx xxxx, Vol. xxx, No. x
uncovers the pathogen-mediated modulation of steroid
homeostasis as a central virulence strategy [102].
Several lines of evidence have also shown that BR
crosstalk with SA regulates plant responses to abiotic
stress. Exogenous application of BRs was unable to confer
salt stress tolerance in the SA-insensitive npr1-1 mutant in
comparison with WT [16]. This result indicated that BR-
induced salt tolerance in Arabidopsis partially depends on
NPR1, a master regulator of the SA-mediated defense
signaling pathway [16]. Recently, exogenous applications
of BRs and SA have been shown to increase salinity stress
tolerance in Brassica juncea. The combined application of
BRs and SA was most effective in alleviating the salt stress
when compared with their individual treatments [103].
BRs and GAs
Recent research has supported the existence of extensive
crosstalk between BRs and GAs in a wide range of biologi-
cal processes, including plant development and responses
to environmental stimuli [102,104]. The GAST family is
critically involved in GA signaling. OsGSR1, a member of
the GAST family in rice, is induced by GA and suppressed
by BRs [104]. RNAi plants with reduced OsGSR1 expres-
sion exhibited reduced sensitivity to GAs, enhanced level of
GAs, reduced levels of endogenous BRs and a dwarf phe-
notype that could be rescued by exogenous BR application.
OsGSR1 was shown to activate BR biosynthesis through
direct interaction with DWF1, suggesting that OsGSR1 is
a probable crosstalk point in GA and BR signaling path-
ways. Another piece of evidence showing the negative
crosstalk of BRs with GAs is the enhanced stabilization
of OsSLR1 by exogenous BR treatment. OsSLR1 is the only
DELLA GA-signaling repressor in rice, which functions as
a key negative regulator in the resistance to P. gramini-
cola. Additionally, expression of OsSLR1 is upregulated in
response to both pathogen infection and exogenous BR
treatment. These data suggest that BRs may antagonize
the GA-induced defense responses in rice through inter-
ference with GA signaling [102]. In contrast to the antago-
nistic crosstalk of BRs and GAs, the impact of BRs on
cotton (Gossypium hirsutum) DELLA genes in fiber cell
initiation and elongation was shown to be positive. Exoge-
nous BR treatment triggers the downregulation of four
DELLA genes in cotton fiber cells, including GhGAI1,
which is engaged in fiber cell initiation [105]. Taken to-
gether, these reports demonstrate that the crosstalk
between BRs and GAs is complex and warrants future
investigation.
Biotechnological manipulation of BR actions to improve
stress tolerance
Exogenous applications of BRs are widely used to improve
stress tolerance in plants [77] (Figure 3b) and the applica-
tion of BRs alone or in conjunction with other PGRs has
become a routine stress management protocol [15,103,106].
Treatment of cucumber (Cucumis sativus) with BRs has
been reported to enhance tolerance to photo-oxidative and
cold stresses and is accompanied by H2O2 accumulation and
systemic induction of genes associated with stress
responses, such as MAPK1 and MAPK3 [17,18]. Similarly,
application of BRs to radish (Raphanus sativus) improves
TRPLSC-983; No. of Pages 12
Review
Table 1. BR metabolic and BR signaling genes involved in stress responses
Gene ID Description Regulatory function in stress response
AtBRI1 BR receptor kinase Negative
AtBAK1 Coreceptor of BRI1 Positive
AtBKK1 BKK1/SERK4, a homolog Positive
of BAK1
AtBZR1 BR transcription factor Positive
AtDWF4 BR biosynthetic gene Positive
OsSERK1 Ortholog of BAK1 in rice Positive
OsGSK1 Ortholog of BIN2 in rice Negative
Abbreviations: At, Arabidopsis thaliana; BAK1, BRI1-ASSOCIATED RECEPTOR KINASE 1; BIN2, Brassinosteroid insensitive 2; BKK1/SERK4, BAK1-like kinase1; BRI1,
BRASSINOSTEROID INSENSITIVE 1; BZR1, BRASSINAZOLE RESISTANT 1; DWF4, DWARF4; GSK1, glycogen synthase 3-like protein kinase; Os, Oryza sativa; SERK, somatic
embryogenesis receptor kinase; TCV, Turnip crinkle virus.
tolerance to Cu and Cr stress owing to the upregulation of a
protective antioxidant system and the modulation of endog-
enous ABA, Aux and polyamine profiles. These results
highlight the existence of crosstalk between BRs and
ABA or Aux in stress responses [107,108]. Furthermore,
the positive effect of BRs in Cr detoxification can be signifi-
cantly improved with the addition of the polyamine spermi-
dine, indicating that the advantageous interplay between
BRs and polyamines may serve as a promising approach to
enhance the mitigation of abiotic stresses in plants [109].
The influence of BRs on stress responses has led to
several biotechnological strategies to enhance plant toler-
ance to abiotic and biotic stresses (Table 1). Seed-specific
overexpression of AtDWF4 in Arabidopsis enhanced cold
tolerance, which was attributed to the upregulation of the
cold-responsive gene COR15A [110]. Loss-of-function of
OsGSK1, a BIN2 homolog of rice, improved tolerance to
cold, heat, salt and drought stresses when compared with
the WT [111]. These data suggest that BR signaling com-
ponents may also serve as potential targets for genetic
engineering of abiotic stress tolerance. The induction of
selective BR signaling components by biotechnological
approaches can also enhance disease resistance. For in-
stance, constitutive overexpression of OsSERK1, a BAK1
homolog of rice, led to an increase in the resistance of
transgenic rice plants to blast fungus [112], while loss-of-
function of BAK1 in Arabidopsis enhanced susceptibility to
Turnip crinkle virus (TCV) infection [113]. The effects of
BRs on stress tolerance depend on the concentration of the
BRs that were applied under the test conditions. Excessive
use of BRs may exert detrimental consequences on the
adaptive responses of plants because appropriate levels of
BRs are required for optimal BR signaling [12,14,31,114]; a
phenomenon that has also been observed with CKs [96].
Concluding remarks
Although recent research has elucidated the BR signaling
pathway from the receptor to BZR1 and BES1, the key
regulators of BR-induced responses in plants, the mecha-
nisms behind the pleiotropic action of BRs and the execu-
tion of BR-induced responses still remains poorly
understood at this time. The versatile role of BRs may
be attributed to multilayer interactions with other PGRs
affecting the post-transcriptional fate of the target
response. Taken together, forward genetic approaches
Trends in Plant Science xxx xxxx, Vol. xxx, No. x
Type of stresses Refs
Immunity response, cold [12,114]
Immunity response, TCV infection, [11,113]
cell death and chlorosis
TCV infection, cell death and chlorosis [113]
Cold [120]
Cold [110]
Disease resistance [112]
Cold, heat, salt, and drought [111]
combined with genome-wide transcriptional analyses
have identified several hundreds of BR targets, shedding
additional light on the complexity of the diverse activity of
BRs in plants. Concerted and focused efforts by the re-
search community are required to further elucidate the
mechanisms of BRs in innate immunity, stomatal devel-
opment and crosstalk with other PGRs to acquire or confer
abiotic and biotic stress tolerance. Furthermore, the high
redundancy of BR signaling components demands addi-
tional attention to clarify the functional roles of the mech-
anisms involved with BR signaling in plants. An
important challenge in the coming years will be unravel-
ing the exact mechanism of the BR-regulated gene net-
work in a systems biology-based manner [115,116].
Challenges ahead will also include uncovering the cross-
talk behavior of BR signaling components with other
PGRs under various stresses. Given the huge potential
and value of BRs in stress management, targeted genetic
engineering of BR biosynthesis and/or BR signaling is
likely to become a popular tool in the coming years to
improve stress tolerance, and perhaps biomass and yield
of agricultural crops [117–119]. As a result, it is hoped that
advances in this area of BR signaling could bring us one
step closer to meeting the demands for increased food
production to feed the growing world population.
Acknowledgments
We apologize to those colleagues who have contributed to this field but
were not cited because of space limitations. This work was supported by a
grant (No. AP24-1-0076) from the RIKEN Strategic Research Program for
R & D to L-SPT. SPC and J-QY are grateful to the support from the
National Basic Research Program of China (2009CB119000).
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