Báo cáo khoa học: Plant oxylipins: COI1/JAZs/MYC2 as the core jasmonic acid-signalling module pptx

MINIREVIEW
Plant 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:
(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.
4682 FEBS Journal 276 (2009) 4682–4692 ª 2009 The Authors Journal compilation ª 2009 FEBS
Parallel 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.
Mutant Gene Major phenotype Refs
coi1 At2g39940, F-box component of
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]
A. Chini et al. COI1/JAZs/MYC2: the core JA-signalling module
FEBS Journal 276 (2009) 4682–4692 ª 2009 The Authors Journal compilation ª 2009 FEBS 4683
rally 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, deg-
COI1/JAZs/MYC2: the core JA-signalling module A. Chini et al.
4684 FEBS Journal 276 (2009) 4682–4692 ª 2009 The Authors Journal compilation ª 2009 FEBS
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 SCF
COI1
to 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 best 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
A. Chini et al. COI1/JAZs/MYC2: the core JA-signalling module
FEBS Journal 276 (2009) 4682–4692 ª 2009 The Authors Journal compilation ª 2009 FEBS 4685
different 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
DGL gene, 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
JAZ3 JAZ9 JAZ10
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 ( />[67]. The gene expression in root cells
types, flowers and the whole plant show
significant tissue-specific differences.
COI1/JAZs/MYC2: the core JA-signalling module A. Chini et al.
4686 FEBS Journal 276 (2009) 4682–4692 ª 2009 The Authors Journal compilation ª 2009 FEBS
Aux ⁄ 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
SCF
TIR1
TIR1
Aux/IAA

Aux/IAA
ARFs
ARFs
Auxin responsive genes
26S
proteasome
Aux/IAA
Aux/IAA
JA signalling
AB
MYC2
MYC2
JA responsive genes
Other TFs?
26S
proteasome
SCF
SCF
COI1
COI1
J
A
Z
J
A
Z
?
JA-Ile
JAZ
JAZ

Ethylene signalling
EIN3
EIN3
Ethylene responsive genes
26S
proteasome
Ethylene
SCF
SCF
EBF
EBF
EIN3
EIN3
PIFs
PIFs
GA responsive genes
26S
proteasome
GA signalling
GA
SCF
SCF
SLY1
SLY1
DELLA
DELLA
GID1
GID1
DELLA
DELLA

CD
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 SCF
COI1
, 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 SCF
SLY1
,
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].
A. Chini et al. COI1/JAZs/MYC2: the core JA-signalling module
FEBS Journal 276 (2009) 4682–4692 ª 2009 The Authors Journal compilation ª 2009 FEBS 4687
A 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 transcriptional 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
SCF
COI1
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 autoregulated
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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