Download Brassinosteroid signal transduction – choices of signals and receptors

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TRENDS in Plant Science
Vol.9 No.2 February 2004
Brassinosteroid signal transduction –
choices of signals and receptors
Zhi-Yong Wang and Jun-Xian He
Department of Plant Biology, Carnegie Institution, 260 Panama Street, Stanford, CA 94305, USA
Small signaling molecules that mediate cell–cell communication are essential for developmental regulation
in multicellular organisms. Among them are the steroids and peptide hormones that regulate growth in
both plants and animals. In plants, brassinosteroids
(BRs) are perceived by the cell surface receptor kinase
BRI1, which is distinct from the animal steroid receptors. Identification of components of the BR signaling
pathway has revealed similarities to other animal and
plant signal transduction pathways. Recent studies
demonstrated that tomato BRI1 (tBRI1) perceives both
BR and the peptide hormone systemin, raising new
questions about the molecular mechanism and evolution of receptor –ligand specificity.
All multicellular organisms have evolved mechanisms to
perceive and respond to extracellular chemical signals,
including endogenous hormones and external cues from
the environment, pathogens and symbiotic organisms.
Among these signaling molecules, steroids and small
peptides are widely used in both animals and plants [1,2].
Although plant and animal steroids have many similarities in biosynthesis and function, the molecular
mechanisms of steroid perception and signal transduction
appear to be different in the two kingdoms. The plant
steroid hormones brassinosteroids (BRs) are perceived by
the cell surface receptor kinase BRI1 [3]. By contrast, most
animal steroid responses are mediated by the nuclear
receptor family of transcription factors [4]. Although some
animal steroid responses are mediated by cell surface
receptors [5], recent cloning of membrane-bound steroid
receptors in fish and mammals indicated that they are
similar to the G-protein-coupled receptors [6,7] but
distinct from the BR receptors. However, the BR signaling
pathway shares features with peptide hormone signaling
pathways in animals and plants. Recent studies in tomato
demonstrated that tomato BRI1 (tBRI1) functions as the
receptor for both BR and systemin, a peptide hormone that
mediates systemic responses to wounding by insect pests
[8]. These studies raise the possibility of conserved
interaction among the BR signaling, defense response
and peptide signaling pathways. Our aim here is to
highlight the latest findings in BR and related signaling
pathways that can provide some insight into the molecular
mechanism of BR signal transduction and plant growth
regulation.
Corresponding author: Zhi-Yong Wang ([email protected]).
Genetic studies identified brassinosteroid signaling
components
BRs are a class of plant steroid hormones with important
regulatory roles in multiple developmental and physiological processes, including seed germination, stem
elongation, leaf expansion, xylem differentiation, disease
resistance and stress tolerance [9 – 11]. BR-deficient
and -insensitive mutants show various developmental
defects, including reduced seed germination, dwarfism,
dark-green and curled leaves, reduced fertility, delayed
reproductive development, and development of lightgrown morphology (de-etiolation) in the dark [3]. Similar
phenotypes can be caused by BR biosynthetic inhibitors,
such as brassinazole (Brz) [12]. By contrast, overexpression of BR biosynthetic enzymes and the BRI1 receptor
increases cell elongation and plant growth [13,14].
Molecular genetic studies of BR response mutants in
Arabidopsis have led to the identification of a BR receptor
and downstream signaling components. Genetic screens
for BR-insensitive mutants have identified multiple alleles
of the bri1 [15,16] and bin2 loci [17 – 19], which led to the
identification of BRI1 as the BR receptor [16] and BIN2 as
a negative downstream regulator [20]. BR-insensitive
mutants have also been identified in other species,
including pea [3], rice [21], barley [22] and tomato [23],
and these mutants have been found to contain mutations
in the BRI1 homologs. The det3 mutant also has dwarf and
de-etiolated phenotypes, and is partially insensitive to
BR. DET3 encodes a subunit of the vacuolar Hþ-ATPase
(V-ATPase), suggesting that V-ATPase activity is involved
in the BR response [24].
Mutants that suppress BR-deficient or -insensitive
phenotypes have also been identified in various genetic
screens. An activation-tagging screen for suppressors of
the weak bri1-5 allele identified genes that promote BR
response when overexpressed. These include the BRS1
gene, which encodes a putative serine carboxypeptidase
[25], and the BAK1 gene, which encodes a leucine-richrepeat (LRR) receptor kinase [26]. BAK1 was also
identified as a BRI1 interacting protein [27]. Genetic
screens for mutants insensitive to the BR biosynthetic
inhibitor Brz and for bri1 suppressors identified the
brassinazole resistant1-D (bzr1-1D) and bri1 EMS suppressor (bes1-D) mutants, respectively [28,29]. Cloning of
BZR1 revealed a close homolog in Arabidopsis named
BZR2, and subsequent sequencing of the BZR2 gene in the
bes1-D mutant revealed that mutations of the same amino
acid residue in BZR1 and BZR2 were responsible for the
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bzr1-1D and bes1-D mutants, respectively [28,29]. These
studies identified BZR1 and BZR2/BES1 as two homologous nuclear proteins that play overlapping yet distinct
roles in BR signaling [28,29] (Figure 1).
Brassinosteroid receptors
BRI1 is an LRR receptor-like kinase (LRR-RLK) located on
the cell surface [16]. BRI1 has an extracellular domain
containing 25 LRRs, a transmembrane domain, and a
cytoplasmic serine/threonine kinase domain [30,31]. It has
been shown that BRI1 immunoprecipitates with BR
binding activity and BR induces autophosphorylation of
BRI1 in vivo [13]. Furthermore, BR binding and kinase
activation is abolished by a mutation in the extracellular
domain of BRI1 [13]. These experiments demonstrate that
BRI1 perceives the BR signal through its extracellular
domain and initiates a signal transduction cascade
through its cytoplasmic kinase activity [13,32].
BAK1 is potentially another component of the BR
receptor complex [26,27,33]. BAK1 interacts with BRI1
in vitro and in vivo, and they phosphorylate each other
in vitro. Results of both gain-of-function and loss-offunction experiments support a positive role for BAK1 in
BR signaling [33]. The molecular mechanism by which BR
activates the receptor kinases is unclear. Although in vivo
interaction between BRI1 and BAK1 has been detected,
the effect of BR on this interaction is not known. Thus, the
hypothesis remains to be tested that ligand binding might
BR
?
BAK1
BRS1
BRI1
?
BR
BR
synthesis
CPD
BIN2
BZR1
BZR2/BES1 + P
BR-regulated
gene expression
V-ATPase
BZR1– P
BZR2/BES1– P
Degradation
by proteasome
Cell wall enzymes
Growth response
TRENDS in Plant Science
Figure 1. A diagram of the brassinosteroid (BR) signal transduction pathway in
Arabidopsis. BR is perceived by the receptor complex containing BRI1 and BAK1,
which are leucine-rich-repeat receptor-like kinases (LRR-RLKs) that interact with
each other. Activation of the receptor kinases by BR binding leads to the dephosphorylation and accumulation of the nuclear proteins BZR1 and BZR2/BES1, possibly by inhibiting the negative regulator BIN2. In the absence of BR, the BIN2
kinase phosphorylates BZR1 and BZR2/BES1, and targets them for degradation by
the ubiquitin-dependent proteasome pathway. BZR1 and BZR2/BES1 regulate BRtarget genes differently; these targets include the BR biosynthetic gene CPD, which
is feedback inhibited by BR through BZR1, and genes encoding enzymes for cell
wall synthesis that are probably regulated by both BZR1 and BZR2/BES1. The
vacuolar Hþ-ATPase (V-ATPase) is also a mediator of certain BR responses. The
serine carboxypeptidase BRS1 is proposed to process an unknown extracellular
factor that contribute to the activation of the BR receptors.
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Vol.9 No.2 February 2004
activate the kinases by inducing receptor heterodimerization, as known for the receptor tyrosine kinases and the
transforming growth factor b receptor kinases in animals
[26,33]. Because BR binding activity was not detected for
recombinant BRI1 proteins expressed in non-plant cells
[13] and BR treatment did not increase receptor phosphorylation nor association between BRI1 and BAK1 coexpressed in yeast cells [27], it is believed that either
proper modification of the receptor kinases or additional
proteins are required for BR binding and signaling. The
BRS1 serine carboxypeptidase has been proposed to
proteolytically process an extracellular component of the
BR receptor complex [25]. Biochemical purification of all
proteins associated with the BRI1 –BAK1 receptor kinase
complex should provide further insight into the molecular
mechanism of the BR receptor function.
Downstream brassinosteroid signaling
Although the direct substrates of BRI1 and BAK1 are
unknown, components further downstream have been
identified. BIN2 encodes a cytoplasmic protein kinase
homologous to the Drosophila SHAGGY kinase and the
mammalian glycogen synthase kinase 3 (GSK3) [20].
Genetic studies indicated that BIN2 is a negative regulator in the BR signaling pathway, similar to most
SHAGGY/GSK3 kinases in animal systems [18,20]. Two
nuclear proteins, BZR1 and BES1, were recently identified
as positive regulators of the BR signaling pathway
downstream of bin2. The accumulation of BZR1 and
BES1 is increased by BR treatment and by the same
mis-sense mutations in bzr1-1D and bes1-D, which
suppress the bri1 and bin2 mutants [28,29]. BZR1 and
BES1 are mostly in phosphorylated forms, and BR
treatment induces dephosphorylation and accumulation
of the proteins [28,29].
Biochemical studies indicate that BIN2 directly phosphorylates and destabilizes BZR1 and BES1 [29,34,35].
BIN2 interacts with BZR1 and BES1 in yeast two-hybrid
assays and phosphorylates them in vitro. In the gain-offunction bin2 mutant, the accumulation of BZR1 and
BES1 is decreased and their BR-induced dephosphorylation is attenuated [29,34]. Phosphorylated BZR1 appears
to be degraded by the 26S proteasome, because treatment
of seedlings with the proteasome inhibitor MG132 preferentially increased the accumulation of the phosphorylated BZR1 protein [34]. MG132 treatment did not alter
the kinetics of BR-induced BZR1 dephosphorylation,
suggesting that BZR1 might be dephosphorylated by a
phosphatase [34].
These studies illustrate a BR signal transduction
pathway leading from the cell surface receptors to the
nucleus (Figure 1). BR activation of the BRI1– BAK1
receptor kinases inhibits BIN2 through an unknown
mechanism, allowing accumulation of unphosphorylated
BZR1 and BES1, which in turn regulate BR target genes in
the nucleus [29,34]. In the absence of BR, BIN2 kinase
inhibits downstream BR responses by phosphorylating
BZR1 and BES1, and targeting them for degradation by
the proteasome (Figure 1) [34]. The regulation of BZR1 and
BES1 degradation by BIN2 phosphorylation is similar to
several signaling pathways in both animals and plants.
Review
TRENDS in Plant Science
Particularly, the structural homology between BIN2 and
GSK3 highlights the similarity to the Wnt signaling
pathway in animals [36]. However, regulated degradation
of nuclear factors by the proteasome has been observed in
various plant signaling pathways and has emerged as a
common theme of signal transduction in plants (Table 1).
The biochemical function of BZR1 and BES1 has yet to
be determined. It is unclear whether BR regulates
transport of BZR1 and BES1 into the nucleus [28,29,35].
Both bzr1-1D and bes1-D mutants have altered expression
of BR-regulated genes [28,29], but it is not known whether
BZR1 and BES1 directly bind to DNA or regulate gene
expression by interacting with DNA-binding proteins. The
different phenotypes of light-grown bzr1-1D and bes1-D
suggest that the two proteins have overlapping yet distinct
functions and thus should have different downstream
targets. A better understanding of the functions of the
BZR1 and BES1 proteins should be achieved by identifying
their interacting proteins, which could include the
phosphatase that dephosphorylates them, the ubiquitin
ligase that targets the phosphorylated BZR1 and BES1 for
ubiquitination and degradation, and possibly transcription factors that interact with BR-regulated promoters.
Tomato BRI1 has dual functions as receptor of
brassinosteroid and systemin
A similar BR signaling mechanism is apparently conserved
in other plants because mutations in BRI1 homologs are
responsible for BR-insensitive mutant phenotypes in pea [3],
rice [21], barley [22] and tomato [23]. Interestingly, recent
studies in tomato demonstrated that tBRI1 is not only
required for BR response but also functions as the receptor
for systemin [37], which is a peptide hormone that mediates
systemic wound responses in tomato partly through inducing jasmonic acid synthesis [38].
Using radiolabeled systemin, Justin Scheer et al.
identified a 160-kDa plasma membrane protein that
bound systemin with high affinity [39], and purified a
putative systemin binding protein using photoaffinity
labeling [37]. Surprisingly, the identified protein, SR160,
was most homologous to BRI1 in Arabidopsis [37], and
mutations in this gene were later found in the tomato
BR-insensitive mutants altered brassinolide sensitivity1
(abs1) and curl3 (cu3) [23], indicating that SR160 is the
BRI1 ortholog tBRI1 [23].
Scheer et al. have recently confirmed that tBRI1/SR160
is the systemin receptor by expressing the tomato
systemin in tobacco and analysing systemin response in
the cu3 mutant [8]. Systemin is present only in members of
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Vol.9 No.2 February 2004
the Solaneae subtribe of Solanaceae family, including
tomato and potato, and is absent from tobacco, a member of
the Nicotianae subtribe. Wild-type tobacco has neither
binding activity nor response to tomato systemin. However, tobacco cells transformed with the tomato tBRI1/
SR160 gene showed systemin binding activity and a
systemin-induced alkalinization response, similar to that
of tomato cells [8]. These results indicate that tBRI1/
SR160 is sufficient to confer systemin responsiveness on
tobacco and that the downstream components of the
systemin signaling pathway are present in tobacco [38].
Furthermore, the BR-insensitive tomato line cu3 has
greatly reduced response to systemin [8]. Although BR
does not inhibit systemin binding to tBRI1 in suspensioncultured tomato cells [37], it reversibly antagonized systemin response in tomato leaves [8]. These studies have
established that tBRI1/SR160 functions as receptor for both
BR and systemin [8]. This exciting conclusion raises many
interesting questions. For example, how can one receptor
kinase perceive two hormones with such different physiological functions [40], and how is specificity achieved for both
ligand recognition and downstream signaling? Furthermore, why does systemin use BRI1 among the hundreds of
LRR-RLKs in plants? Is tBRI1 a special case or are BR
receptors of other plants also bifunctional, perceiving both
steroidal and peptide ligands?
One receptor for two signals
The only other receptor known to perceive two types of
ligands is the mammalian oxytocin receptor (OTR), a
member of the G-protein-coupled-receptor family. OTR
binds to both the peptide hormone oxytocin and the steroid
hormone progesterone [41]. In this case, oxytocin and
progesterone antagonistically regulate similar physiological responses by competing for binding to the same
receptor [41]. The regulation of BRI1 by BR and systemin
appears to involve a mechanism different from the
oxytocin – progesterone systems. First, loss-of-function
mutation of tBRI1 inactivates both BR and systemin
responses, indicating that BRI1 is a positive regulator for
both pathways and should be activated by both ligands [8].
Second, BR does not reduce systemin binding [37] but does
inhibit the systemin response [8], suggesting that BR
binds to different ligand-binding sites and inhibits
systemin response by recruiting tBRI1 from the systemin
pathway into the BR signaling pathway (Figure 2).
If systemin competes with BR for tBRI1, one might
expect systemin to act as an inhibitor of growth. Interestingly, the transgenic tomato plants that overexpress the
Table 1. Common theme in plant signal transduction – signal for degradation of key nuclear regulators by the proteasome
Signals
Nuclear factor and functiona
E3 ligase
Effect of the signal
Refs
Brassinosteroid
Auxin
BZR1 (þ)
Aux and IAAs (2 )
NAC1 (þ)
GAI, RGA and SLN1 (2 )
ABI5 (þ)
Unknown
Hy5 (þ)
Unknown
TIR1
SINAT5
SLY1
AFP?b
COI1
COP1
Accumulation
Degradation
Accumulation
Degradation
Accumulation
Unknown
Accumulation
[34]
[55]
[56]
[57,58]
[59]
[60]
[61]
Gibberellins
Abscisic acid
Jasmonic acid
Light
a
Activation of plant signal transduction pathways often leads to degradation of repressors (2) or accumulation of activators (þ ) in the nucleus by regulating the interaction
between the nuclear protein and specific ubiquitin E3 ligases that promote its ubiquitination and degradation by the proteasome.
The biochemical function of AFP is unknown.
b
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(b) Tomato
(a) Drosophila
Wounding
Pathogen or
developmental
signals
Spaetzle
BR
BR
Toll
Systemin
Prosystemin
Pro-Spaetzle
BAK1?
tBRI1
?
tBRI1
Pelle
Plasma
membrane
tBRI1
JA
Embryo
polarity
Defense
response
Cell wall synthesis
Growth responses
Defense response
TRENDS in Plant Science
Figure 2. The similarities between the brassinosteroid (BR) and systemin signaling pathways in tomato and the Toll signaling pathways in Drosophila. (a) The Toll signaling
pathway controls both embryonic development and innate immunity in Drosophila. Toll is a large transmembrane receptor with an N-terminal extracellular leucine-richrepeat (LRR) region similar to that of the BRI1 receptor kinase in plants and a C-terminal intracellular (TIR) domain. Toll is activated by binding of its ligand Spaetzle. Spaetzle is synthesized as an inactive precursor, which is processed and activated by proteases generated either during embryo development or upon pathogen invasion of adult
flies. The binding of Spaetzle to Toll induces dimerization of the receptor and activation of the downstream kinase Pelle, a serine/threonine kinase evolutionarily related to
the kinase domain of BRI1. Activation of Pelle leads to dorsoventral polarity gene expression during embryo development and defense gene expression in innate immune
responses of adult flies. (b) BR signaling (left) and systemin signaling (right) pathways in tomato. tBRI1 perceives both BR and systemin signals. BR interacts with the extracellular domain of BRI1 and activates the kinase activity of BRI1, initiating a signaling cascade that leads to BR-regulated gene expression and growth responses. The tBRI1
receptor complex might also contain BAK1. Systemin is produced from a precursor protein prosystemin by proteolytic processing upon wounding. Systemin binds to the
tBRI1 to initiate a signaling pathway that leads to systemic defense responses by inducing jasmonic acid (JA) synthesis. Jasmonic acid also feeds back to induce systemin
and tBRI1, further amplifying and spreading the signals. BR inhibits systemin responses, suggesting that the two signals compete for the receptor to regulate developmental or defense responses.
pro-systemin gene (35S-Prosys) have significantly longer
hypocotyls than wild-type plants [42], suggesting that
systemin promotes seedling growth. However, the longhypocotyl phenotype of 35S-Prosys plants is unlikely to be
caused by direct activation of the BR signaling pathway.
Mutants that suppress the accumulation of protease
inhibitors also suppress the long-hypocotyl phenotype of
35S-Prosys tomato. These include the suppressors of
prosystemin-mediated responses 2 (spr2) mutant, which
is blocked in jasmonic acid biosynthesis [43], suggesting
that prosystemin promotes growth through a jasmonic
acid-dependent pathway. Jasmonic acid might affect
growth directly or by feedback regulating systemin and
tBRI1 activity. Jasmonic acid feedback activates prosystemin [38,44] and systemin binding activity [39] to amplify
and spread the systemic signals efficiently. The specificity
of downstream responses might vary with developmental
stages, as known for the dual-functional Drosophila Toll
receptor (see below).
of Dorsal nuclear localization, leading to embryonic
polarity [47]. In innate immunity of adult flies, recognition
of bacteria and fungi by the peptidoglycan-recognition
proteins triggers a proteolytic cascade that ultimately
cleaves inactive Spaetzle into a shortened activated form,
which activates Toll and leads to the production of
antimicrobial peptides that mediate defense [48]. In
addition to Spaetzle and Toll, some downstream components (Tube, Pelle and Cactus) are required for both
developmental and defense responses [45]. Active Spaetzle
binds to Toll directly with high affinity and with a
stoichiometry of one Spaetzle dimer to two receptors,
thus activating Toll by inducing receptor dimerization
[49]. The dual function of tBRI1 in developmental and
defense responses is thus similar to Toll. Unlike Toll, which
is activated by the same ligand Spaetzle, tBRI1 apparently
perceives both BR and systemin. Thus, tBRI1 appears to
be the only receptor known to be activated by two signals
that lead to two distinct responses.
One receptor for two responses
The dual function of tBRI1 is similar to that of the
Drosophila receptor Toll, which also has an extracellular
LRR domain structurally similar to that of BRI1. Toll is
essential for establishing dorsoventral patterning in
embryos as well as for innate immune defenses to fungi
and bacteria in adult flies [45]. During embryo development, binding of Toll by its ligand Spaetzle leads to
activation of the Pelle kinase, which is evolutionarily
related to the kinase domain of BRI1 [46], and nuclear
translocation of the transcription factor Dorsal. The
asymmetric generation of Spaetzle results in a gradient
Perspectives and prospects
LRR-containing receptors are conserved in plants, insects
and mammals for mediating innate immunity [50,51].
Homologs of Toll (Toll-like receptors, TLRs) have been
found in mammals to mediate both innate and adaptive
immune responses. Mammalian TLRs perceive not only
exogenous molecules from microorganisms but also
endogenous agonists such as the degradation products of
macromolecules, products of proteolytic cascades and
intracellular components of ruptured cells [52]. It has
been proposed that TLRs represent an ancient mechanism
of perceiving environmental challenges and cellular
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damage [52]. Whereas most animals have fewer than a
dozen LRR receptors, plants have evolved with an
expanded family of more than 500 LRR proteins. These
include , 210 Arabidopsis LRR-RLKs containing a cytoplasmic kinase domain related to Pelle [46], some of which
are known to function in disease resistance [53] and
developmental regulation [54]. The dual function of tBRI1
might represent an evolutionarily conserved mechanism.
It has been proposed that BRI1 might have a defensive role
that was co-opted by systemin during evolution in the
Solaneae subtribe of the Solanaceae family [38]. Although
systemin is only found in a subtribe of Solanaceae plants,
various peptides that induce similar cellular responses
have been found in other plants [38], and proteolytic
processing of peptides has been implicated in BR signaling
in Arabidopsis [25]. It is possible that BRI1 in Arabidopsis
and other plants also perceives peptide signals and has a
role in defense.
Whereas it might be wise for Drosophila to use one
receptor efficiently for two responses, it is surprising that
the dual functions of tBRI1 have not separated after such
dramatic expansion of this receptor gene family in plants.
There is possibly a benefit for coupling BR and wounding
signals with one receptor, such as coordinating cell expansion with cell wall synthesis in order to avoid cell rupture.
Signals generated by cell damage can regulate either cell
wall synthesis or defense responses, perhaps depending on
the developmental stage of the tissue. Systemin might
have evolved recently from a local wounding signal that
became jasmonic acid inducible or from a jasmonic acidinduced peptide that acquired tBRI1 binding activity.
Further studies of BR and systemin signaling in tomato
will shed light on the specificities of LRR-RLKs at the
levels of both ligand binding and downstream signaling.
Like the Toll pathway, some of the downstream components might also be shared between BR and systemin
responses, and it will be interesting to determine whether
BAK1, BIN2, BZR1 and BES1 play roles in systemin
signaling. Conversely, analysis of BR responses of the
other systemin-related tomato mutants and identification
of systemin signaling components will provide a better
understanding of how the specificity of downstream
signaling is achieved. The questions about the mechanism
of dual function remain to be answered by further studies
of the BRI1 receptor complex. Perhaps a more important
question is whether the dual function has been evolutionarily conserved. The wound and BR responses are two of
the best-studied plant signaling pathways, and their
merging promises to bring more excitement in the future.
Acknowledgements
We thank David Ehrhardt, Yu Sun and Zhiping Deng for critical reading of
the manuscript. Research on BR signal transduction in Z-Y.W.’s laboratory
is supported by Carnegie Institution and the National Institute of Health.
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18th International Plant Growth Substances Conference
20–24 September 2004
Canberra, Australia
For more information, please see http://www.conlog.com.au/ipgsa2004/
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