Keywords arabidopsis; COI1; hormone response; Jas domain; jasmonate signalling; JAZ repressors; MYC2; transcription factors; ZIM domain Correspondence R.. Abbreviations ARF, auxin respon
Trang 1Plant oxylipins: COI1/JAZs/MYC2 as the core jasmonic
acid-signalling module
Andrea Chini, Marta Boter and Roberto Solano
Departamento de Gene´tica Molecular de Plantas, Centro Nacional de Biotecnologı´a-CSIC, Madrid, Spain
Introduction
Plants are sessile organisms that need to adapt to their
constantly changing environment The specific plant
response to a particular stimulus, crucial for its survival
and fitness, is mediated by a complex hormonal network
Jasmonates (JAs) are essential signalling molecules
modulating the plant response to biotic and abiotic
stresses as well as several growth and developmental
traits [1–4] In general, JAs help to modulate the
com-petitive allocation of plant energy to defence or growth,
the two major processes determining plant fitness
Dissection of the jasmonic acid (JA) pathway has
been predominantly carried out using genetic studies
The Arabidopsis coi1 mutant was originally identified
as insensitive to coronatine (COR), a bacterial com-pound structurally related to JAs [5,6] coi1 plants are defective in all JA-dependent responses tested, demon-strating the central role of COI1 in the JA-signalling pathway [7] COI1 encodes an F-box protein Proteins containing an F-box domain are components of the Skp⁄ Cullin ⁄ F-box (SCF)-type E3 ubiquitine ligase complexes conferring substrate specificity Mutations
in additional components or regulators of SCF com-plexes such as AXR1, CUL1, RBX and JAI4⁄ SGT1b also show JA insensitivity, further supporting the importance of protein degradation in activating the JA pathway (Table 1) [8–12]
Keywords
arabidopsis; COI1; hormone response;
Jas domain; jasmonate signalling; JAZ
repressors; MYC2; transcription factors; ZIM
domain
Correspondence
R Solano, Departamento de Gene´tica
Molecular de Plantas, Centro Nacional de
Biotecnologı´a-CSIC, Campus Universidad
Auto´noma, 28049 Madrid, Spain
Fax: +34 91 585 4506
Tel: +34 91 585 5429
E-mail: rsolano@cnb.csic.es
(Received 7 November 2008, revised
3 February 2009, accepted 20 February
2009)
doi:10.1111/j.1742-4658.2009.07194.x
Jasmonic acid (JA) and its derivates, collectively known as jasmonates (JAs), are essential signalling molecules that coordinate the plant response
to biotic and abiotic challenges, in addition to several developmental pro-cesses The COI1 F-box and additional SCF modulators have long been known to have a crucial role in the JA-signalling pathway Downstream JA-dependent transcriptional re-programming is regulated by a cascade of transcription factors and MYC2 plays a major role Recently, JAZ family proteins have been identified as COI1 targets and repressors of MYC2, defining the ‘missing link’ in JA signalling JA–Ile has been proposed to be the active form of the hormone, and COI1 is an essential component of the receptor complex These recent discoveries have defined the core JA-signal-ling pathway as the module COI1⁄ JAZs ⁄ MYC2
Abbreviations
ARF, auxin response factor; bHLH, basic helix-loop-helix; COR, coronatine; ERF, ethylene response factor; GA, gibberellin; IAA, indole-3-acetic acid; JA, jasmonic acid; Me-JA, methyl ester of JA; OPDA, 12-oxophytodienoic acid; PIF, phytochrome interacting factor; SCF, Skip ⁄ Cullin ⁄ F-box; TF, transcription factor.
Trang 2Parallel genetic screens for JA-insensitive mutants
identified jin1, carrying a mutation in the MYC2 gene,
another key component of the JA-signalling pathway
[10,13,14] MYC2 encodes a basic helix-loop-helix
(bHLH) transcription factor (TF) that recognizes the
G-box and G-box variants in the promoter of its target
genes and regulates different branches of the JA
path-way [10,14–18] MYC2 induces JA-mediated responses
such as wounding, inhibition of root growth, JA
bio-synthesis, oxidative stress adaptation and anthocyanin
biosynthesis In addition, MYC2 represses other
JA-mediated responses such as tryptophan metabolism
and defences against necrotrophic pathogens
[10,14,17] However, ethylene-response-factor 1
(ERF1) and other ERFs, such as ORA59, integrate JA
and ethylene signals, and regulate some of the
MYC2-modulated responses in an opposite fashion [10,19,20]
More recently, several independent groups have
identified the JAZ family of repressors in Arabidopsis
by genetic screens and microarray analyses [16,21,22]
JAZ proteins are direct targets of COI1 that are
degraded by the 26S proteasome in response to the
hormone Furthermore, JAZ proteins also directly
interact with MYC2 repressing its activity, and
there-fore function as repressors of the JA pathway [16,23]
Discovery of the JAZ family led to the identification
of the first core signalling module in the JA pathway:
COI1–JAZs–MYC2 [3,16], which is the focus of this
minireview Moreover, the similarities between JA and
other hormone-signalling pathways such as those of
auxins, gibberellins or ethylene are also discussed These similarities suggest a common strategy to trans-duce hormonal signals in plants, based on the regula-tion of protein stability by the ubiquitin–proteasome pathway
JA perception and the nature of the active hormone
Despite multiple biochemical and genetic efforts, the molecular details of hormone perception have been utterly shielded until recently COI1 is essential for all known JA-dependent responses and, intriguingly, the closest COI1 homologues among the 700 Arabidop-sis F-box proteins are the auxin receptors TIR1⁄ AFBs [24–26] The critical role of COI1 in all JA responses and the acknowledged similarity between the JA and auxin pathways suggest that COI1 might be the long-sought JA receptor [16,27,28]
The identification of the JA receptor is intimately correlated to the nature of the ligand molecules The
JA biosynthetic pathway ends with the production of
JA and the methyl ester of JA (Me-JA), long consid-ered the bioactive molecules [4,29–31] Characteriza-tion of the JA-insensitive jar1 mutant identified JAR1
as an enzyme catalysing the conjugation of JA to amino acids (preferentially Ile) [32–35] Although jar1 mutants are defective in some JA responses, these defects are complemented by external application of JA–Ile, revealing the biological relevance of this
natu-Table 1 SCF and COP9 Arabidopsis mutants impaired in JA signalling.
the SCF E3 ubiquitine ligase complexes
Reduced root growth inhibition and anthocyanin accumulation by JA and coronatine Male sterile
[5,7]
axr1 At1g05180, RUB-activating enzyme E1 Reduced root growth inhibition by
JA Reduced expression of VSP, Thi1.2 and PDF1.2 upon JA treatment
[12,94]
eta3 ⁄ jai4 At4g11260 ⁄ SGT1b modulator of
the SCF complex
Reduced root growth inhibition by JA [9,10]
fus6 ⁄ CSN1-11 At3g61140 ⁄ CSN1, subunit 1 of the
COP9 complex involved in protein deneddylation
Reduced root growth inhibition by
JA Reduced expression of PDF1.2 upon JA treatment
[95]
cul1 ⁄ axr6 At4g02570 ⁄ CULLIN1, cullin protein
of the SCF complex
Reduced root growth inhibition by JA [11,96] AtRBX1 RNAi At5g20570 ⁄ RBXA, ring-box 1-like
protein
Reduced root growth inhibition by
JA Reduced expression of VSP and AOS upon JA treatment
[12,97]
CSN5 RNAi At1g22820 ⁄ CSN5A, subunit of the
COP9 complex involved in protein deneddylation
Reduced root growth inhibition by
JA Reduced expression of VSP upon JA treatment
[97]
Trang 3rally occurring JA derivative and suggesting that JA is
not active per se [4,33–38]
Recent reports have shown that JA–Ile directly
induces the interaction between COI1 and several JAZ
proteins at physiological concentrations, whereas none
of the tested precursors or intermediates, such as
12-oxophytodienoic acid (OPDA), Me-JA or JA, can
promote the interaction [21,23,39] (S Fonseca et al.,
unpublished results) Taken together, these results
con-firm that JA–Ile has all the essential characteristics of
a bioactive molecule
Direct JA–Ile and COR induction of the COI1⁄
JAZs interaction provides a framework to identify the
JA receptor The binding of radiolabelled COR by
tomato cellular extracts requires COI1 [39] Thus,
extracts from null coi1 mutants failed to recover any
radiolabelled COR Similarly, a point mutation
(L418F) in the COI1 region corresponding to the
auxin-binding pocket of TIR1 decreases the recovery
of radiolabelled COR [39] In addition, JA–Ile and
COR are recognized by the same receptor, because
JA–Ile can compete with radiolabelled COR for
bind-ing to the extract [39] More recently,
immunoprecipi-tated COI1 has been proved to interact with different
JAZ proteins in a hormone-dependent manner,
indi-cating that either COI1, or a protein co-purifying
with COI1, is the COR⁄ JA–Ile receptor (S Fonseca
et al., manuscript submitted) As expected for a
hor-monal receptor, the COI1⁄ JAZs interaction is dose
dependent, reversible and very quick Moreover, the
expression of COI1 and JAZ proteins in yeast is
suffi-cient for hormone-dependent yeast responsiveness and
growth [21,23] (S Fonseca et al., unpublished results)
In summary, several independent lines of evidence
strongly support that COI1 or the COI1⁄ JAZ
com-plex is the COR and JA–Ile receptor However, direct
binding between COI1 and the hormone has not been
reported and the structural resolution of the COI1–
hormone–JAZ complex is crucial to reveal the
molec-ular details of the hormone perception
In addition to Ile, JAR1 can conjugate JA to other
amino acids (Val, Leu, Ala, Phe, Met, Thr, Trp and
Gln), although less efficiently [33] Similar to JA–Ile,
JA–Val, JA–Leu and JA–Ala are also naturally
occur-ring molecules able to directly induce a COI1⁄ JAZ
interaction in tomato cell extract and whose external
application triggers specific JA-dependent plant
responses [21,33,39] In contrast to the bioactive JA–
Ile, however, JA–Val, JA–Leu and JA–Ala fail to
induce JA-dependent root growth inhibition in the
Arabidopsis jar1 mutant, demonstrating that, at least
in Arabidopsis, these JA–amino acid conjugates are not
active as such, but require a functional JAR1 to
acti-vate JA-dependent responses [33] (S Fonseca et al., unpublished results) Therefore, in Arabidopsis, JA–Ile
is the only bioactive JA identified to date and JAR1 is essential for producing this hormone Of note, several jar1 alleles and knockout lines show a residual JA–Ile presence suggesting partial redundancy in the JAR1 function, as already shown in tobacco [33,34,40] Despite its importance, JA–Ile is the first, but proba-bly not the only, bioactive JA For example, Arabidop-sis opr3 mutants, unable to convert OPDA into JA, are deficient in several JA-regulated responses such as growth inhibition and fertility, but not in activating defence responses [41] OPDA also induces the expres-sion of several JA-responsive genes, as well as a specific sub-set of JA-independent genes, confirming the ability of OPDA to trigger plant responses distinct
to JA [42,43] In addition, JA–Ile treatment of JAR4⁄ 6-silenced tobacco plants, deficient in JA–Ile produc-tion, is able to re-establish the natural resistance response to Manduca sexta However, application of JA–Ile fails to restore the defence response in LOX3-silenced plants, lacking JA–Ile and other oxylipins [40] These data suggest that other oxylipins, in addition to JA–Ile, are responsible for triggering JA-mediated defence responses and, therefore, the existence of addi-tional bioactive JAs can be expected
JAZ repressors: the JA-pathway hub
JAZ proteins represent the molecular connection between COI1 and MYC2; the three proteins defining the core JA-signalling module In Arabidopsis, the JAZ protein family consists of 12 members sharing two conserved motifs, ZIM and Jas Loss of the Jas motif
in JAI3⁄ JAZ3 (the jai3-1 mutant) causes dominant JA insensitivity, indicating the relevance of this motif for the regulation of this protein function [16] Consis-tently, constitutive expression of truncated forms of JAZ1, JAZ3 and JAZ10 lacking the Jas motif also generates JA-insensitive plants [16,21,22] In vivo deg-radation studies have shown that at least three JAZ proteins, JAZ1, JAZ3 and JAZ6, are degraded by the 26S proteasome in a COI1-dependent manner upon
JA treatment Yeast two-hybrid and pull-down assays showed that, in the presence of the hormone, COI1 physically interacts with JAZ1, JAZ3 and JAZ9 via their Jas motif in a dose-dependent manner, and that two positively charged amino acids within this motif are essential for the interaction [21,23,39] (S Fonseca
et al., manuscript submitted) Truncated JAZ deriva-tives (lacking the Jas motif) consistently lose this hor-mone-dependent binding to COI1 and are resistant to JA-induced degradation [16,21,23,39] Therefore,
Trang 4deg-radation of JAZ proteins is essential to de-repress the
JA pathway
Continuous repression of their TF targets by these
degradation-resistant JAZ derivatives has been
proposed to explain the mechanism by which they
promote dominant JA insensitivity [21,23] However,
this explanation is unlikely because the Jas motif is
also required for the interaction with MYC2 [16,23]
(S Fonseca et al., unpublished results) In contrast to
COI1, the interaction of JAZ proteins with MYC2
does not depend on the presence of the hormone
[16,23,39] Therefore, both COI1 and MYC2 proteins
seem to compete for interaction with the Jas motif,
and the presence of the hormone determines the
out-come of this competition [16] Thus, under basal
con-ditions, the Jas domain of JAZ proteins interacts with
MYC2 and other transcription factors to repress the
JA response Increases in JA–Ile after stress would
promote COI1 binding to the Jas domain of JAZ
proteins, their consequent degradation and the release
of MYC2 and other transcription factors involved in
JA-induced gene expression [16]
Constitutive expression of the truncated version of
JAZ3 prevents JA-dependent degradation of other
JAZ proteins such as JAZ1 and JAZ9, suggesting a
possible alternative explanation for the dominant
JA-insensitive phenotype promoted by truncated JAZs
The mutant JAZ3 protein (retaining the ZIM domain
but lacking the Jas motif) was proposed to partially
inactivate COI1, therefore preventing the degradation
of additional JAZ proteins that continue to repress
their TF targets [16] Crystal structure analyses of
COI–JAZ complexes, identification of new JAZ targets
and characterization of the ZIM domain function will
help to clarify this issue
Consistent with the interaction between JAZ3 and
MYC2, microarray experiments have shown that genes
containing MYC2 DNA-binding sites (the G- and
T⁄ G-boxes) in their promoters and positively regulated
by MYC2 are deregulated in jai3-1 mutants [16]
Therefore, the genetic and molecular data, together
with transcriptional profiling, pinpointed JAZ proteins
as the long-postulated repressors targeted for
protea-some-degradation by SCFCOI1to activate the
JA-regu-lated responses
To date, only MYC2 has been identified as a target of
JAZ repressors However, MYC2 does not regulate all
JA-dependent responses, and therefore, JAZ proteins
are expected to target additional TFs MYC2 belongs to
the large family of bHLH transcription factors (> 160
in Arabidopsis) involved in many different processes,
from stress responses to development [44,45] MYC2
constitutes a master switch regulating abscisic acid and
JA⁄ ethylene responses, as well as blue-light-dependent photomorphogenesis [10,17,46,47] It is tempting to speculate that other bHLHs, structurally related to MYC2, may also be targeted by JAZ proteins to fine-tune specific downstream responses In the recent years, additional TFs belonging to different families such as ERF (ERF1, ORA59, AtERF1, AtERF2, and AtERF4), MYB (MYB21 and MYB24) and WRKY (WRKY70, WRKY18) have also been involved in JA signalling [19,20,48–51] Thus, these TFs and their clos-est homologues represent the bclos-est candidates for JAZ targets to date [17] However, some of these TFs may
be indirectly modulated by MYC2 via a secondary regulatory cascade, such as the case of the NAC transcription factors ANAC019 and ANAC055, whose expression is induced by JA in a MYC2-dependent manner [52]
JAZ family: redundancy and specificity
Functional redundancy among JAZ family members has been inferred from the lack of JA-related pheno-types in individual knockout jaz mutants, with the exception of JAZ10 [21,22] Supporting this redun-dancy, all the COI1-interacting JAZ proteins also inter-act with MYC2 (i.e JAZ1, JAZ3 and JAZ9) [16,23] Moreover, phylogenetic analyses of the JAZ gene fam-ily, the number and position of their introns, as well as their presence in duplicated chromosome segments, show the existence of well-defined JAZ clades [16,21,53] Therefore, although the implication of the JAZ family in regulation of the JA pathway is clear, double or multiple mutants are required to demonstrate the involvement of individual JAZ genes in this path-way, and to clarify their regulation of particular JA responses
Despite their likely redundant function, some speci-ficity in the role of individual JAZ proteins can be expected In fact, different JAs, precursors or mimetics induce specific, as well as overlapping, responses in plants [41–43,54–58] A mechanistic explanation for these specific responses in particular tissues may be based on the promotion of specific COI1⁄ JAZ com-plexes by different bioactive JAs, combined with the fact that different JAZ proteins may target specific TFs, and with the tissue specificity of JAZs and⁄ or their TF targets Thus, specific JAZ degradation in response to a particular jasmonate would determine the activation of a specific module (COI1⁄ JAZ ⁄ TF) and subsequent tissue-specific JA responses [16,21] Although data supporting this hypothesis are scarce, examples can be found in the closely related auxin pathway Thus, the SCF-mediated degradation of
Trang 5different Aux⁄ indole-3-acetic acid (IAA) repressors in
response to specific auxins exhibits different
kinet-ics [59,60] Moreover, specificity in the TF targets
of Aux⁄ IAA genes has also been reported [61–64]
Finally, tissue-specific expression of different Aux⁄
IAA and⁄ or their TF targets has been described
[62,65,66]
Similar to the case of the auxin pathway, JAZ
profiling analyses show very diverse tissue- and
stage-specific expressions (Fig 1) [67] Interestingly, similar
spatial and temporal regulation is also emerging for
the production and accumulation of JA and its
deri-vates Recent metabolite profiling of Arabidopsis plants
showed very dynamic spatial and temporal changes in
the synthesis of JA and its hydroxylated derivates in
response to wounding [68] In addition, a
comprehen-sive ‘jasmonate⁄ oxylipin signature’ analysis, measuring
JA, its precursors and derivates in several plant
species, confirmed their differential accumulation in
specific organs and stages [57,69] Oxylipin inactivation
by hydroxylation and sulfonation may also contribute
to the establishment of these dynamic spatial and
temporal patterns of jasmonate activity [68] Moreover,
an elegant genetic approach has also confirmed this
temporal regulatory mechanism by identifying the
DGLgene, a homologue of DAD1, encoding a
chloro-plastic lipase [70,71] Both enzymes catalyse the
pro-duction of linolenic acid, the first, critical step in JA biosynthesis Although DAD1 and DGL share partial functional redundancy, their differential induction kinetics and organ-specific expression (DAD1 in flow-ers, DGL in leaves) provides them with independent, temporally and spatially separated roles [70] The tis-sue- and stage-specific expression of JAZ genes and their TF targets, combined with the spatially and temporally regulated biosynthesis of bioactive JAs may generate an extraordinary rich signalling repertoire able to modulate very different JA responses despite the likely partial JAZ redundancy
The characterization of lines knocked-out in com-plete JAZ clades, combined with a precise study of JAZ expression patterns and the comprehensive analy-ses of COI1 interaction with all JAZs in the presence
of different bioactive JAs, is required to elucidate indi-vidual JAZ function
Evolutionary success of SCF function
Recent advances in hormone signalling have uncovered
a common strategy in which SCF protein degradation complexes are central for the transmission of hormonal signals in plants (Fig 2) In the case of auxins, IAA and related molecules serve as ‘molecular glue’ bring-ing together the F-box protein TIR1⁄ AFB and the
JAZ1
Stage III
Stage II
Dry seed Dry seed Dry seed Dry seed
Stage I
Stage III
Stage II
Stage I
Stage III
Stage II
Stage I
Stage III
Stage II
Stage I
Fig 1 Tissue-specific expression of repre-sentative JAZ genes The expression of JAZ1, JAZ3, JAZ9 and JAZ10 genes is rep-resented as in the Bio-Array Resource (BAR) database (http://bbc.botany.utoronto.ca/) [67] The gene expression in root cells types, flowers and the whole plant show significant tissue-specific differences.
Trang 6Aux⁄ IAA proteins, resulting in the degradation of
Aux⁄ IAA repressors, which in turn activate the auxin
response by de-repression of auxin response factor
(ARF) transcriptional activators [24,26,72] Similarly,
JA–Ile may also serve as ‘molecular glue’ to promote
the interaction between COI1 and the JAZ proteins,
resulting in JAZ degradation and the consequent
de-repression of JA transcriptional activators such as
MYC2 Both Aux⁄ IAA and JAZ are rapidly induced
by auxins and JA, respectively, and their induction
depends on their respective transcriptional activator
targets (ARFs and MYC2, respectively) providing a
negative regulatory loop that allows to switch off the
response [16,21,73]
Gibberellin (GA) signalling may also fit into this
common strategy, although some variations are
evi-dent Unlike the F-boxes, TIR1 and COI1, the GA
receptor, GID1, has similarity with a
hormone-sensi-tive lipase [74] GA binding to GID1 is required for the interaction of the receptor with DELLA proteins, transcriptional repressors of GA responses [75–79] In turn, GID1–DELLA interaction promotes the recogni-tion of DELLA by the F-box SLY1 resulting in the degradation of DELLA repressors and the de-repres-sion of transcriptional activators of GA-responsive genes like PIF3 and PIF4 [80–82], which belong to the bHLH family, like MYC2 Interestingly, recent findings have shown that a constitutively active domi-nant-negative DELLA mutation, gai, enhances the induction of JA-responsive genes, whereas a quadruple DELLA knockout mutant, which lacks four of the five Arabidopsis DELLA proteins, was partially insensitive
to JA [83] This finding points to a possible role for DELLA proteins in GA⁄ JA signalling cross-talk, although the molecular bases remain unknown
Auxin signalling
Auxins
SCF TIR1 Aux/IAA
ARFs
Auxin responsive genes
26S proteasome
Aux/IAA
JA signalling
MYC2
JA responsive genes Other TFs?
26S proteasome
SCF COI1 JAZ
?
JA-Ile
JAZ
Ethylene signalling
EIN3
Ethylene responsive genes
26S proteasome
Ethylene
SCF EBF EIN3
PIFs
GA responsive genes
26S proteasome
GA signalling
GA
SCF SLY1 DELLA
GID1
DELLA
Fig 2 SCF-dependent proteasome
degra-dation represents a common strategy in
plant hormone signalling (A) In an
un-induced situation, the JAZ proteins repress
MYC2 and additional unknown transcription
factors Upon JA–Ile perception, JAZ
repres-sors are targeted for proteasome
degrada-tion by SCFCOI1, therefore liberating MYC2
and activating the JA responses (B) In the
same way, Aux ⁄ IAA inhibits the ARF
tran-scriptional modulators in the absence of
auxin Increased auxin concentrations
pro-mote SCF TIR1 -mediated degradation of
Aux ⁄ IAAs, which in turn de-repress ARF
transcription factors and auxin responses.
(C) Similarly, at basal GA levels, the DELLA
repressors block phytochrome interacting
factors (PIFs) and additional transcription
factors Following hormone perception,
GID1 mediates the recognition and
degrada-tion of the DELLA repressors by SCFSLY1,
therefore activating PIF transcriptional
mod-ulators and downstream GA responses.
(D) The ethylene pathway is the most
diver-gent situation because, in the absence of
the hormone, the transcriptional activator
EIN3 is constitutively degraded in a
SCF EBF1 ⁄ 2 -dependent manner Upon
ethyl-ene perception, EIN3 is stabilized, thus
activating ethylene responses These
models were adapted from Chico et al [3].
Trang 7A central role for SCF-mediated degradation in
eth-ylene signalling is also well documented [84,85] The
ethylene pathway represents the most divergent
situa-tion because a transcripsitua-tional activator, EIN3, is
constitutively degraded in a proteasome-dependent
manner by direct interaction with two F-box proteins,
EBF1 and EBF2 [86,87] Upon ethylene perception,
EIN3 is stabilized, thus activating ethylene responses
More recently, identification of the novel plant
branching hormones, strigolactones, has been reported
[88,89] Interestingly, one of the key proteins regulating
the branching process is again an F-box, MAX2,
which has been proposed to mediate the degradation
of a repressor in response to the branching hormone
[90–92] If this is the case, the strigolactone pathway
may be very similar to that of auxins, JA and GAs,
providing further evidence of the extraordinary success
of the ubiquitin⁄ proteasome pathway as a strategic
mechanism in plant hormone sensing and signalling
Evolutionarily, auxin, JA, GA and ethylene
percep-tion and signalling pathways would constitute subtle
turns in a unique and highly conserved plant strategy
[3,84,90,93] This mechanism may provide potential
nodes of interaction between different signalling
mole-cules explaining the extraordinary plasticity
intrinsi-cally associated with these pathways
On/off model and future perspectives
The discovery and characterization of the JAZ proteins
describes the first complete JA-signalling module
(COI⁄ JAZ ⁄ MYC2) that helps us understand how JA
responses are turned on and off (Fig 2) Upon
hor-monal perception, JAZ repressors are targeted by
SCFCOI1 for degradation, de-repressing MYC2 and
probably additional TFs These transcriptional
modu-lators activate downstream JA-mediated responses as
well as the expression of most JAZ genes, therefore
re-establishing the MYC2⁄ JAZ repressor complexes
[16] This simple negative feedback loop represents an
efficient regulatory mechanism providing an
appropri-ate response to JA and its subsequent autoregulappropri-ated
deactivation (Fig 2)
Although the discovery of JAZ repressors has paved
the way for understanding the core module responsible
for JA signalling, new questions arise that need to be
addressed if we are to fully understand the fine-tuning
of this core module As described above, the nature of
the active plant hormone is essential to fully appreciate
the details of JA perception JA–Ile is the only
bioac-tive JA identified to date, although the existence of
additional bioactive molecules may be expected The
specific COI1⁄ JAZ interaction provides the molecular
tools with which to test the direct activity of several JAs
An additional layer of regulation in JA signalling may be the intracellular transport of the hormone JAZ repressors, and probably COI1, are nuclear pro-teins and the COI1-dependent degradation of JAZ proteins triggered by the hormone also occurs in the nucleus However, it remains unknown whether the active molecules diffuse or are actively transferred into the nucleus
Finally, the tissue and temporal specificity of JAZ genes expression, in combination with their likely repression of different TFs, may account for the acti-vation of specific JA responses Further analyses of the mechanisms by which JA-signalling modules are temporally and spatially distributed will result in a comprehensive understanding of the complexity of JA-mediated plant responses
Acknowledgements
We thank J.M Chico and S Fonseca for critical reading
of the manuscript Work in RS’s lab is supported by funding from the Ministerio de Educacio´n y Ciencia of Spain, the Comunidad de Madrid and European Com-mission AC was supported by the Juan de la Cierva Programme and an EMBO Long-term Fellowship
Note added in proof
Very recently, two manuscripts have reported that the ZIM domain acts as a protein–protein interaction domain mediating homo- and heteromeric interactions between JAZ proteins (Chung & Howe, 2009 [98,99]) Chung & Howe also propose that JAZ splice variants serve to attenuate signal output in the presence of JA via protein–protein interaction through the ZIM domain These findings provide new clues to under-stand the dominant JA insensitivity conferred by the JAZDJas proteins
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