Modularity in Jasmonate Signaling for Multistress Resilience

PP69CH14_Howe ARI 4 April 2018 11:40

Annual Review of Plant Biology

Modularity in JasmonateSignaling for MultistressResilienceGregg A. Howe,1,2 Ian T. Major,1 and Abraham J. Koo3

1Department of Energy–Plant Research Laboratory, Michigan State University, East Lansing,Michigan 48824, USA; email: [email protected], [email protected] of Biochemistry and Molecular Biology, and Plant Resilience Institute, MichiganState University, East Lansing, Michigan 48824, USA3Department of Biochemistry, University of Missouri, Columbia, Missouri 65211, USA;email: [email protected]

Annu. Rev. Plant Biol. 2018. 69:387–415

First published as a Review in Advance onMarch 14, 2018

The Annual Review of Plant Biology is online atplant.annualreviews.org

https://doi.org/10.1146/annurev-arplant-042817-040047

Copyright c© 2018 by Annual Reviews.All rights reserved

Keywords

jasmonate, JAZ, hormone, plant immunity, crosstalk, transcriptionalregulation, specialized metabolism, effector proteins

Abstract

The plant hormone jasmonate coordinates immune and growth responses toincrease plant survival in unpredictable environments. The core jasmonatesignaling pathway comprises several functional modules, including a reper-toire of COI1–JAZ (CORONATINE INSENSITIVE1–JASMONATE-ZIM DOMAIN) coreceptors that couple jasmonoyl-L-isoleucine perceptionto the degradation of JAZ repressors, JAZ-interacting transcription factorsthat execute physiological responses, and multiple negative feedback loops toensure timely termination of these responses. Here, we review the jasmonatesignaling pathway with an emphasis on understanding how transcriptionalresponses are specific, tunable, and evolvable. We explore emerging evi-dence that JAZ proteins integrate multiple informational cues and mediatecrosstalk by propagating changes in protein–protein interaction networks.We also discuss recent insights into the evolution of jasmonate signaling andhighlight how plant-associated organisms manipulate the pathway to sub-vert host immunity. Finally, we consider how this mechanistic foundationcan accelerate the rational design of jasmonate signaling for improving cropresilience and harnessing the wellspring of specialized plant metabolites.

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ANNUAL REVIEWS Further

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https://www.annualreviews.org/doi/full/10.1146/annurev-arplant-042817-040047


Jasmonate: a generalterm used to refer toJA-Ile, JA, and otherderivatives of thehormone

Jasmonoyl-L-isoleucine ( JA-Ile):the receptor-activeform of jasmonate inhigher plants, which isformed by conjugationof JA to Ile

Jasmonic acid ( JA):the immediate oxylipinprecursor of JA-Ile;plant responses toexogenous JA requireits prior intracellularconversion to JA-Ile

Contents

INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 388THE CORE JASMONATE SIGNALING PATHWAY . . . . . . . . . . . . . . . . . . . . . . . . . . . . 390

Transcriptional Repression. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 390From JA-Ile Perception to Transcriptional Activation . . . . . . . . . . . . . . . . . . . . . . . . . . . . 394

TEMPORAL AND SPATIAL CONTROLS. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 395Time-Delayed Termination of Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 395Organ- and Cell Type–Specific Modules . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 398

THE INTEGRATION OF JASMONATE SIGNALINGAND MOLECULAR CROSSTALK . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 399JAZ Transcriptional Modules . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 399JAZ Proteins As Nodes for Signal Crosstalk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 401Toward a Dynamic JAZ Interaction Network . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 402

THE MANIPULATION OF JASMONATE SIGNALINGBY PLANT-ASSOCIATED ORGANISMS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 402Pathogen Effectors As Receptor Ligands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 403Effectors that Modify JAZ Stability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 404Effectors that Interfere with MYC Transcription Factors . . . . . . . . . . . . . . . . . . . . . . . . . 404

THE EVOLUTION OF JASMONATE SIGNALING. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 404TRANSLATIONAL APPLICATIONS IN JASMONATE RESEARCH . . . . . . . . . . . . 405

INTRODUCTION

Plants continuously integrate environmental signals to adjust their growth, development, andmetabolism in ways that optimize reproductive success. In addition to anticipating diurnal cues,such as light and temperature, plants as sessile organisms benefit from the ability to sense andrespond to unpredictable environmental influences, including water shortage and associations withorganisms that infect, parasitize, or otherwise exploit plants as a source of nutrition and shelter.Through the millennia, these selective pressures shaped the emergence of signaling networksin which small-molecule hormones have a central role in linking stress perception to complextranscriptional responses that promote plant resilience in changing and often hostile environments(37, 119, 131).

Here, we discuss advances in understanding the molecular mechanisms by which the majorstress hormone jasmonate and the receptor-active conjugate jasmonoyl-L-isoleucine ( JA-Ile), inparticular, mediate transcriptional responses to various environmental and developmental cues.As a member of the oxylipin family of compounds, JA-Ile is best known for promoting durableresistance to a broad spectrum of plant consumers, ranging from pathogenic bacteria and fungi toinsect and mammalian herbivores (17, 100). Much of the scientific interest in this field can be tracedto studies showing that jasmonic acid ( JA), methyl-JA (MeJA), and other metabolic precursorsof JA-Ile (referred to collectively as jasmonates) are potent elicitors of specialized metabolitesand proteins that deter plant enemies (14, 48, 65, 128, 154). Given the role of these coevolvingplant–biotic interactions in shaping chemical richness within the plant kingdom (9), we argue thatmechanistic knowledge of the jasmonate pathway and its evolutionary origins will advance a broadunderstanding of patterns of plant defense and, more generally, the ecology of terrestrial habitatsthat are dominated by plants and their interacting organisms. Toward this goal, we build on the

388 Howe · Major · Koo

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JAZy

Input signals and inductive cues

JA-Ile

SCFCOI1

TFa TFb TFc

Plastid lipids Salt stress

Developmental cues Mechanical tissue damage/DAMPs

Physical signals

MAMPs

HAMPs

Temperature extremes

Biotic stress responses • Specialized metabolites

and defense proteins • Volatile attractants

Developmental responses • Growth inhibition • Defensive structures • Reproduction and fertility

Abiotic stress responses • Drought tolerance• Salinity tolerance• Freezing tolerance

Cons

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Integrated response outputs

Signalintegration

Drought

JAZx JAZz

Figure 1Input signals and output responses of the core jasmonoyl-L-isoleucine ( JA-Ile) signaling pathway. Theschematic depicts how the modular design of JA-Ile signaling is linked to various inductive cues (top) andphysiological output responses (bottom). Inductive signals include microbe-, herbivore-, anddamage-associated molecular patterns (MAMPs, HAMPs, and DAMPs, respectively) derived from attackingorganisms, damaged plant cells, and other environmental stresses. These signals are recognized by patternrecognition receptors at the cell surface to trigger de novo synthesis of JA-Ile from plastid lipids. JA-Ilepromotes degradation of multiple JAZ proteins (exemplified by JAZx–z) via the action of the E3 ubiquitinligase SCFCOI1 and the 26S proteasome. Degradation of JAZ relieves repression on the JAZ-interactingtranscription factors (exemplified by TFa–c) that govern various physiological output responses involved ingrowth, development, and tolerance to biotic and abiotic stresses. The conserved core pathway may berepurposed through evolution to link other input signals to specific transcriptional responses. This simplifiedscheme does not depict that many JAZ proteins functionally interact with multiple transcription factors.

JASMONATE-ZIMDOMAIN ( JAZ):a family of nuclearproteins that bind toand repress varioustranscription factors;JAZ proteins alsofunction as part of theJA-Ile receptor

JASMONATE-ZIM DOMAIN ( JAZ) repressor model of induced resistance and extend the ideathat modularity in the core JA-Ile signaling pathway can accommodate evolutionary innovationsthat link various environmental inputs to diverse physiological outputs (Figure 1) (17, 65). Theconserved yet flexible organization of this signaling system is consistent with the remarkablespectrum of defense traits regulated by JA-Ile, as well as increasing evidence that the hormone hascritical roles in ensuring plant tolerance to many abiotic stresses, including high salinity, drought,and temperature extremes (67, 76, 82, 150). Interestingly, the function of jasmonate is not limitedto improving stress tolerance but extends to various aspects of plant growth and reproduction that

www.annualreviews.org • Modularity in Jasmonate Signaling 389

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ZIM domain:a conserved sequencein JAZ proteins thatmediates JAZ homo-andheterodimerizationand also interacts withthe NINJA adaptorprotein

Basichelix-loop-helix(bHLH): a conservedDNA-binding domainpresent in MYC andrelated transcriptionfactors that controljasmonate responses

MYC transcriptionfactors (MYCs): basichelix-loop-helixtranscription factorsthat regulate manyjasmonate-responsivegenes

TIFY: a family ofplant-specific proteinsthat includes JAZ;named for theconservedTIF[F/Y]XG sequencemotif within the ZIMdomain

Jas motif: a conservedsequence near theC terminus of JAZproteins that isinvolved in JA-Ileperception, MYCbinding, and nuclearlocalization

JAZ-interactingdomain ( JID):a structural motif nearthe N terminus ofMYC transcriptionfactors that binds JAZproteins

are integral to stress resilience (14, 154). As illustrated by studies of plant growth–defense trade-offs (60, 68, 131, 185), the dual roles of jasmonate in stress protection and in development areincreasingly viewed not as divorced processes but rather as components of an integrated responsethat optimizes Darwinian fitness in dynamic environments (Figure 1).

The discovery of JAZ proteins a decade ago (26, 148, 168) spurred remarkable progress inunderstanding how the biosynthesis of JA-Ile is coupled to transcriptional activation of jasmonate-responsive genes. Here, our emphasis on JAZ signifies the importance of this protein family inexplaining an overarching question that continues to propel the field forward: How does a singlemajor form of the hormone ( JA-Ile) in vascular plants generate transcriptional outputs that areboth highly specific and yet functionally diverse? We synthesize recent genetic and structuralstudies through the lens of JAZ proteins to describe both the core JA-Ile signaling pathway as wellas a larger network of protein–protein interactions that underpin molecular crosstalk in jasmonatesignaling. We also discuss recent insights into the ancient origins of jasmonate signaling andthe emerging paradigm that core pathway components are frequent targets for manipulationby diverse organisms that depend on plants as a source of nutrition. Finally, we describe howpresent knowledge of JA-Ile action is laying the foundation for addressing important challengesin translational research that will help meet global demands for food security and the sustainableproduction of valuable plant products.

THE CORE JASMONATE SIGNALING PATHWAY

The core jasmonate signaling pathway consists of interconnected functional modules that governthe transcriptional state of hormone-responsive genes. The most intensively studied jasmonate-inducible transcription factors are the basic helix-loop-helix (bHLH) protein MYC2 and its closerelatives, such as Arabidopsis MYC3 and MYC4; these members of bHLH subclade IIIe bind toG-box motifs to regulate the expression of a large portion of jasmonate-responsive genes (26, 39,79, 101). Here, we review progress made in the past decade in understanding the mechanismsby which MYC transcription factors (MYCs) are subject to JAZ-mediated repression and JA-Ile-triggered activation.

Transcriptional Repression

The plant-specific group of JAZ proteins plays a critical part in repressing the activity of MYCtranscription factors. JAZ proteins belong to the larger family of TIFY proteins that is namedfor the presence of a highly conserved TIF[F/Y]XG motif residing within the ZIM (initiallynamed for a zinc-finger protein expressed in the inflorescence meristem) domain of all familymembers (Figure 2) (7, 151). The JAZ repressors are distinguished from other TIFY proteinsby the presence of an approximately 27-amino-acid, multifunctional Jas motif located near theC terminus (Figures 2 and 3a). Interspecies variation in the number of JAZ genes, which rangesfrom one in Marchantia polymorpha to more than 20 in many higher plants, reflects whole-genomeand tandem duplication events that gave rise to functional diversity and redundancy in this rapidlyevolving gene family (7). The Arabidopsis genome encodes 13 JAZ proteins ( JAZ1–JAZ13) thatare classified into 5 phylogenetic groups (I–V) (Figure 2) (149). These five groups are present inall angiosperms, with significant expansion of group I JAZ proteins in monocots (7).

When cellular levels of JA-Ile are below a threshold concentration, the Jas motif adopts an ex-tended α-helix conformation that binds to the JAZ-interacting domain ( JID) near the N terminusof MYCs (Figure 3a,b) (175). Although the JID and adjacent transactivation domain (TAD)of MYC2 were initially mapped as discrete regions (79), structural analysis of JAZ9–MYC3


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V

TIFY (ZIM) EAR Divergent TIFY

Jas CMID

IV

I

MYC2 COI1 GroupJAZTIFYArabidopsisgene locus NINJA TPL

II

III

Conserved intron

AT3G22275 JAZ13

JAZ8TIFY5aAT1G30135

JAZ7TIFY5bAT2G34600

JAZ1 TIFY10aAT1G19180

JAZ2 TIFY10bAT1G74950


JAZ6 TIFY11bAT1G72450

AT5G20900 TIFY3b JAZ12

AT5G13220.1 TIFY9 JAZ10.1



AT1G70700 TIFY7 JAZ9

AT1G48500 TIFY6a JAZ4

AT3G17860 TIFY6b JAZ3

Mapoly0097s0021 MpJAZ


Jas, divergentdegron

Direct interactionNo or weak interactionNo data available

Figure 2The JAZ protein family in Arabidopsis. The phylogenetic tree includes JAZ proteins encoded by 13 loci (JAZ1–JAZ13) and the singleJAZ found in Marchantia polymorpha (MpJAZ; the broken structure indicates that the N and C termini of MpJAZ are larger thanshown). Also depicted are two splice variants of JAZ10 in which the Jas motif is truncated ( JAZ10.3) or deleted ( JAZ10.4) relative tothe full-length JAZ10.1 variant. Many other JAZ derivatives are generated by alternative splicing, but they are not shown for simplicity.Phylogenetic groups I–V denote the major JAZ subclades in angiosperms (7). The position of conserved functional domains is depictedby colored boxes. JAZ13 was not initially identified as a TIFY protein (151), but nevertheless it contains a recognizable but highlydivergent TIFY (ZIM) signature. Inverted black triangles denote positions of conserved introns that flank the Jas motif in thecorresponding genomic DNA. Alternative splicing events involving retention of the second of these introns can result in truncation ofthe Jas motif and greatly reduced interaction with COI1 (e.g., JAZ10.3) (28). Both the Jas motif and the cryptic MYC-interactiondomain (CMID) bind to MYCs. Several JAZ proteins (e.g., JAZ8) contain an EAR motif that mediates direct interaction with TPL.The right side of figure summarizes protein–protein interaction data for each JAZ with MYC2, COI1 (in the presence of JA-Ile),NINJA, and TPL (cyan, direct interaction; gray, no or weak interaction; white, no data for MpJAZ interactions).

Mediator complexsubunit 25 (MED25):a subunit of theMediator complex thatinteracts with MYCtranscription factors,COI1, and chromatin-modifying enzymes

complexes revealed that the JID and TAD functionally overlap to form a continuous groove thatencompasses the Jas helix (175). Structural, biochemical, and in planta analyses indicate that the Jashelix competitively inhibits MYC binding to the activator interacting domain (ACID) of MED25of the Mediator complex, which is an evolutionarily conserved, multiprotein complex that bridgesDNA-bound transcription factors and RNA polymerase II, and integrates transcription with awide variety of cellular signals. A proposed model in which JAZ binding to the JID–TAD regionobstructs MYC3–MED25 coupling and, thereby, represses the expression of jasmonate-responsivegenes (175) is consistent with studies showing that MED25 is a positive regulator of jasmonate re-sponses (20, 22, 81). An and coworkers (4) reported that MED25 and JAZ1 can simultaneously bind


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Mediator complex:a multisubunitcomplex that regulatesthe transcriptionalstatus of jasmonate-responsive genes

MYC2 in its resting (i.e., repressed) state and, consistent with the JAZ–MED25 competition model(175), also showed that MED25–MYC2 interactions are enhanced upon JA-Ile elicitation (4).

The discovery of JAZ10 alternative splice variants that lack the Jas motif (Figure 2) but retainthe ability to repress jasmonate responses suggested that additional JAZ sequence determinantsare involved in MYC repression (28, 29). Indeed, structure–function analyses showed that JAZ10harbors a cryptic MYC-interaction domain (CMID) near the N terminus (108). X-ray crystallog-raphy studies comparing the structure of the MYC3–JAZ10CMID and MYC3–JAZ10Jas complexesshowed that whereas the Jas motif binds MYC3 as a single continuous α-helix, the CMID adoptsa bipartite structure in which one α-helix occupies the Jas-binding groove of MYC and a sec-ond helix makes contact with the backside of this groove (174). This clamp-like action of theCMID engages MYC3 with higher affinity than the Jas helix does and also effectively masks the

COI1

MED25

TPL

TPL

CO

COI1

c

Transcriptional activation(high JA-Ile)

• Defense response• Developmental response • Negative feedback

26S proteasome

UbUb Ub Ub

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JA-Ile catabolism

TF competition

Stable JAZ

MYC

MYC

Signalattenuation

b

Pol II

JA-Ile

MYC COI1

JA-Ile

G-box

a

Jas motif–encoding exon COI1-boundJas domain:

coreceptor function

MYC-boundJas domain:

repressor function

NINJA

NINJA

COI1

CoR

JAZ

Derepression(high JA-Ile)

Repression(low JA-Ile)

JAZ

2255555

MYC

JAZ

MED25

MED25

HAC1

Pol II

MYC

MYC

555MYC

JAM

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27

+ + + + + + + + +

(Caption appears on following page)


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Figure 3 (Figure appears on preceding page)

Model of transcriptional regulation by jasmonoyl-L-isoleucine ( JA-Ile). (a) Sequence logo of the canonical Jas motif of JAZ proteins.Horizontal red bar indicates amino acid residues at the N terminus of the Jas motif that form a loop that traps JA-Ile in the ligandbinding pocket of COI1 (135). + symbols denote the major MYC-interacting residues in the MYC3–JAZ9Jas complex (175). Verticalblack arrows denote the location of highly conserved introns, which in many JAZ genes flank an exon that encodes the N-terminalapproximately 20 amino acids of the Jas motif (28). (b) Simplified model depicting the JA-Ile-induced conformational change in the Jasmotif of JAZ proteins. When bound to MYC in the absence of JA-Ile (left), the motif adopts an extended α-helix conformation thatbinds to and represses MYC transcription factors (MYCs). When bound to COI1 in the presence of JA-Ile (right), the Jas motif adopts abipartite structure (C-terminal helix and N-terminal loop) that is integral to the hormone coreceptor complex. This conformationalchange appears to underlie the JA-Ile-dependent conversion of MYCs from repressors to transcriptional activators. (c) The schematicdepicts the effect of intracellular JA-Ile levels on the transcriptional state of jasmonate-responsive genes. Low JA-Ile levels (top left)permit the accumulation of JAZ proteins that bind and repress MYCs. Repression of jasmonate-responsive genes involves indirectrecruitment of TPL via JAZ-bound NINJA and potentially other corepressors (CoR) as well. Some JAZ proteins contain EAR motifsfor direct binding of TPL (not shown; see Figure 2). In response to signals that trigger JA-Ile accumulation, the hormone ( yellow star)promotes JAZ binding to the COI1 component of SCFCOI1, polyubiquitylation of JAZ, and subsequent degradation of JAZ by the 26Sproteasome. (Bottom right) JAZ degradation unmasks the MED25 binding site on MYC to engage the Mediator complex (blue ovals) andrecruit additional coactivators (e.g., HAC1), resulting in formation of the transcription preinitiation complex with RNA polymerase II(Pol II; strong gene expression denoted by thick arrow). (Bottom left) Many jasmonate-responsive genes encode components involved insignal attenuation, including JA-Ile catabolic enzymes, stable JAZ proteins (such as JAZ8, JAZ13, and JAZ10.4) that are recalcitrant toCOI1 interaction, and JAM transcription factors (TF) that compete with MYC for binding to G-box motifs (orange box) in thepromoter region of target genes (weakened gene expression denoted by thin arrow). These negative feedback loops terminate jasmonateresponses with a characteristic time delay and eventually restore the repressive state.

Cryptic MYC-interaction domain(CMID): thisstructural domainbinds MYCtranscription factorswith high affinity andis found in a subset ofJAZ proteins

TOPLESS (TPL):a tetramericcorepressor proteinthat interacts withEAR motifs found inNINJA, some JAZproteins, and manyother transcriptionalregulators

Ethylene-responsefactor amphiphilicrepression (EAR)motif: a shortsequence motif foundin NINJA and someJAZ proteins thatbinds the corepressorTOPLESS

MED25 binding site of this MYC transcription factor. Functional CMIDs have been identified inother Arabidopsis JAZ proteins (e.g., JAZ1) and likely exist in other plants as well (Figure 2) (55,174). These collective findings provide an unprecedented structural view of how distinct modulardomains of JAZ (CMID and Jas) interact with and repress MYC activity, and they establish a con-ceptual foundation on which to evaluate JAZ-mediated repression of transcription factors otherthan MYC.

JAZ proteins also attenuate MYC activity through recruitment of the TOPLESS (TPL)scaffolding protein that silences gene expression through interactions with histones; chromatin-modifying enzymes, such as histone deacetylase (HDA); and the Mediator complex (80, 115). TPLand TPL-related (TPR) proteins interact specifically with ethylene-response factor amphiphilicrepression (EAR) motifs found on a wide range of transcriptional repressors (19). The TIFY (ZIM)domain of most JAZ recruits TPL or TPR proteins indirectly through the EAR motif–containingNOVEL INTERACTOR OF JAZ (NINJA) adaptor protein (Figures 2 and 3) (115). A subsetof JAZ proteins (e.g., JAZ8) contains EAR motifs that bind TPL directly to repress jasmonateresponses independently of NINJA (Figure 2) (137, 147). The role of TPL as a general repressorof gene expression, together with the ability of non-JAZ TIFY proteins to recruit NINJA–TPLcomplexes via the TIFY (ZIM) motif (33), indicates that these corepressor modules are not specificto jasmonate signaling but, rather, are shared among diverse transcriptional complexes.

Dimerization and higher-order multimerization of MYC (39, 95), JAZ (25, 29), and TPL(80) family members are consistent with the view that transcriptional repression of jasmonate-responsive genes involves large multiprotein complexes (46). There is evidence to indicate thatthese complexes exert epigenetic effects by navigating transcriptional constraints imposed by chro-matin (4, 38, 97). The RPD3-type histone deacetylase HDA6, for example, directly interacts withJAZ proteins and represses the expression of several jasmonate responses in Arabidopsis (82, 160,184). Conversely, MED25 recruits HAC1 to catalyze histone 3 Lys 9 (H3K9) acetylation near thetranscriptional start sites of MYC2 target genes (4). Understanding the relationship between jas-monate signaling and the dynamics of chromatin remodeling is a promising area for future researchthat has the potential to uncover mechanisms underlying the control of specialized metabolism,


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NOVELINTERACTOR OFJAZ (NINJA): anadaptor protein thatrecruits TPL to mostJAZ proteins torepress gene targets ofMYC and othertranscription factors

CORONATINEINSENSITIVE1(COI1): an F-boxprotein that binds JAZsubstrates in thepresence of JA-Ile,resulting in JAZubiquitination anddegradation

transgenerational resistance, signal priming, and other functional aspects of plant resilience toenvironmental stress (101, 126).

From JA-Ile Perception to Transcriptional Activation

A critical step in JA-Ile-triggered signal transduction is the proteolytic destruction of JAZ repres-sors, which effectively converts JAZ-bound MYCs from repressors to transcriptional activators.The first step in this chain of events involves the hormone-dependent formation of a corecep-tor complex consisting of JA-Ile, JAZ, and the F-box protein CORONATINE INSENSITIVE1(COI1) (Figure 3). COI1 is a component of a SKP1–CUL1–F-box protein (SCF) E3 ubiquitinligase complex (SCFCOI1) that interacts specifically with its JAZ substrates in the presence of JA-Ile (75, 148, 161, 166). The three-dimensional structure of the COI1–JAZ coreceptor complexrevealed that the Jas motif has a bipartite structure in which a short conserved degron sequence(ELPIARR in JAZ1) at the N terminus of the motif forms a loop that traps JA-Ile in the ligandbinding pocket via multiple direct contacts, thus forming a stable COI1–JA-Ile–JAZ ternary com-plex (Figure 3a,b) (135). The C terminal region of the Jas α-helix appears to dock the Jas peptideto the surface of COI1. JAZ proteins that are recruited to SCFCOI1 in this hormone-dependentmanner are tagged with polyubiquitin chains and subsequently degraded by the 26S proteasome(Figure 3). Consistent with this structural model (135), JAZ proteins harboring a mutated degronare stable in the presence of JA-Ile and exert dominant repression on MYC activity (26, 31, 103,148, 157, 168). COI1 itself is subjected to multiple levels of regulation, including direct associationwith an essential inositol polyphosphate cofactor (89, 109, 135) and regulated proteolysis (164).

JA-Ile-induced destruction of JAZ by the SCFCOI1-proteasome system provides an efficientmechanism to dissociate corepressor modules (e.g., NINJA–TPL) from the promoters of MYCtarget genes and subsequently recruit transcriptional coactivators. Biochemical and structuralstudies indicate that JAZ degradation simultaneously unmasks JID and TAD to permit binding ofMED25 and engagement of RNA polymerase II via the Mediator complex, thus establishing anactivated transcriptional state (Figure 3). This emerging model of hormone-dependent relief ofrepression on MYC is supported by genetic, biochemical, and structural studies (14, 41, 86, 116). Aremarkable feature of this mechanism is the key part played by structural changes in the Jas motif,which makes direct contact with COI1, JA-Ile, and MYC. It appears that changes in JA-Ile levelsare associated with distinct conformations of the Jas motif as it exists in the MYC–JAZ restingcomplex (175) compared with the hormone-activated COI1–JAZ complex (135), thus providinga simple switch to derepress MYC activity (Figure 3b). Rapid (<15 min) expression of primarytarget genes in response to increased JA-Ile levels (30, 52, 85) attests to the speed of transcriptionalactivation and is consistent with the short half-life of some JAZ repressors, such as JAZ1 (56, 115,148). Direct binding of COI1 to a multiprotein repression complex containing JAZ-bound MYCmay increase the efficiency of hormone-dependent JAZ degradation, thus linking JA-Ile perceptionto the RNA polymerase II general transcription machinery assembled at the promoters of MYCtarget genes (Figure 3c) (4).

Sequence variation in the JAZ degron affects JAZ stability and the physiological outputs ofthe jasmonate pathway (137, 149). This observation supports a scenario in which combinatorialassembly of COI1 with various JAZ coreceptors that exhibit a range of destruction kinetics mayprovide a mechanism to sense a dynamic range of JA-Ile concentrations, analogous to the presentview of discriminatory auxin perception (16). In this manner, specific input signals that triggerthe accumulation of discrete thresholds of JA-Ile in the nucleus could conceivably activate specifictranscription factors as a mechanism to increase response specificity (27, 137). In addition to inter-actions with JAZ, MYC and other JAZ-interacting transcription factors are subject to many other


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levels of posttranslational regulation, including phosphorylation (172) and polyubiquitylation (73).This complexity of regulation likely reflects extensive crosstalk between signaling pathways thatconverge on MYC and other JAZ-associated transcription factors (24, 79, 136).

TEMPORAL AND SPATIAL CONTROLS

Core components of the jasmonate signaling pathway are subject to many layers of regulationthat serve to tailor the amplitude, duration, and developmental timing of responses, as well as theexpression of cell-type and organ-specific JAZ–transcription factor modules. Insight into thesespatial and temporal control circuits is critical for understanding the broader role of this hormonein governing physiological trade-offs, crosstalk with other signaling pathways, and general patternsof defense and specialized metabolism in the plant kingdom.

Time-Delayed Termination of Signaling

Although innate immune responses are essential to staving off plant consumers, these reactionscan be detrimental to host fitness if not appropriately terminated, for example, when a threatsubsides or when responses to multiple stresses must be prioritized. It is also well documentedthat jasmonate-triggered immunity is antagonistically linked to growth and reproductive physi-ology (60, 185). Accordingly, inducible transcription factors, such as MYC, that execute immuneresponses should be active for only defined periods following induction. This functionality ismediated by negative feedback loops that operate with built-in time delays, including negativeregulators whose production is stimulated by inducible transcription factors (127). In this con-text, it is noteworthy that many negative regulators of jasmonate signaling have been identifiedusing coexpression-based guilt-by-association approaches that have proven remarkably powerfulfor exploring the jasmonate network (17).

JA-Ile catabolism and transport. Jasmonate-mediated transcriptional responses are tightly in-tegrated with the accumulation of JA and JA-Ile, whose production from fatty acid precursors inchloroplast membranes has been extensively studied (Figure 4) (83, 130, 154). A key feature ofJA-Ile as the molecular trigger of signaling is its rapid accumulation (a timescale of seconds tominutes) in response to tissue damage or other types of elicitation (52, 85). Initial insights intometabolic pathways that switch off signaling came from observations that the wound-induced JAburst is followed by a rapid decline in hormone levels, concomitant with the accumulation ofhydroxylated JA derivatives (105). Studies over the past several years have uncovered a metabolicnetwork that efficiently removes the cytosolic pools of JA-Ile generated by the JA-conjugatingenzyme JAR1 (61, 83, 87, 143).

At least three major pathways catabolize JA-Ile or restrain its production in the cytosol(Figure 4). In the ω-oxidation pathway, cytochromes P450 in the CYP94 subfamily catalyzethe sequential oxidation of JA-Ile to 12OH-JA-Ile and 12COOH-JA-Ile (62, 84, 88). In the hy-drolysis pathway, members of the amidohydrolase family catabolize JA-Ile to JA and Ile (10, 156,158, 178). JA-Ile accumulation is also curtailed by enzyme systems that divert the flux of JA fromJAR1. JA oxidases (called JOX or JAO) belonging to the 2-oxoglutarate dioxygenase family oxidizeJA to 12OH-JA as an efficient restraint on JA-Ile production (Figure 4) (15, 138). The conversionof JA to volatile methyl-JA by JA carboxyl methyltransferase provides another metabolic route fordepleting JA pools and thus reducing JA-Ile accumulation (134, 144).

In addition to this intricate metabolic grid for maintaining JA-Ile homeostasis, jasmonate re-sponses are also regulated by the transport of the hormone within and between cells. Li and


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JA-Ile-lactone

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(3R,7S)-JA-L-Ile(+)-7-iso-JA-L-Ile

Figure 4Major pathways for jasmonoyl-L-isoleucine ( JA-Ile) metabolism and related structures. (a) Major metabolic pathways for JA-Ilehomeostasis. Jasmonic acid ( JA) is synthesized from linolenic acid (18:3) via the octadecanoid pathway, which involves both the plastidand peroxisome. JA is metabolized to various bioactive and nonbioactive derivatives. The volatile methyl JA (MeJA) is formed by JAcarboxyl methyltransferase ( JMT), whereas the reverse reaction is catalyzed by MeJA esterase (MJE). JAR1 conjugates Ile to JA to formthe major bioactive hormone, JA-Ile (see the sidebar titled Bioactive Jasmonates). Consecutive oxidation of the pentenyl side chain ofJA-Ile by CYP94 subfamily cytochromes P450 produces 12OH-JA-Ile and 12COOH-JA-Ile. Amide bond cleavage of JA-Ile and itsoxidized derivatives by amidohydrolases (IAR3 and ILL6) produces JA or 12OH-JA, together with the amino acid moiety. JA is directlyconverted to 12OH-JA by JA-induced oxygenases ( JOXs or JAOs) (15, 138). 12OH-JA can be further metabolized to sulfated(12HSO4-JA) or glucosylated (12-O-Glc-JA) derivatives. The O-glucosyl derivative (12-O-Glc-JA-Ile) of JA-Ile as well as glucosylesters (not shown) of both JA and JA-Ile also occur. Evidence that JA-Ile entry into the nucleus involves a transporter ( JAT1) impliesthe existence of discrete nuclear ( JA-Ilenuc) and cytosolic ( JA-Ilecyt) pools of the hormone (92). JA efflux transporters including but notlimited to JAT1 also localize to the plasma membrane to mediate the cellular efflux of JA. (b) Structures of naturally occurring plantjasmonates, pathogen-derived JA-Ile mimics, and synthetic analogs of JA-Ile. JA-Ile [also known as (3R,7S)-JA-L-Ile or(+)-7-iso-JA-L-Ile] is the major bioactive form of the hormone and may epimerize to a more thermodynamically stable but less active(3R,7R)-JA-L-Ile stereoisomer (not shown). Naturally occurring structural mimics of JA-Ile include pathogen-derived coronatine(COR) and the Ile-conjugated form (CFA-Ile) of coronafacic acid (CFA). A synthetic O-methyloxime derivative of COR (COR-MO)antagonizes COI1–JAZ interaction (107), whereas the synthetic macrolactone ( JA-Ile-lactone) has properties of a receptor agonist (72).


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BIOACTIVE JASMONATES

Bioactive jasmonates are endogenous oxylipins that promote the formation of COI1–JAZ coreceptor complexes.Nonbioactive compounds are either metabolic precursors (e.g., JA) or catabolic derivatives of receptor-active jas-monates (Figure 4). Initial studies showed that JA-Ile, but not JA, methyl-JA, or OPDA, mediates COI1 binding toJAZ (75, 103, 148), thereby extending pioneering work on the JA-conjugating enzyme JAR1 as a positive regulator ofthe pathway (143). The use of pure stereoisomers in subsequent research, including a high-resolution crystal struc-ture of the COI1–JA-Ile–JAZ complex, showed that (+)-7-iso-JA-Ile is the most active naturally occurring isomerowing to the cis configuration of bonds at C3 and C7 of the cyclopentanone ring (Figure 4) (42, 135). Structurallyrelated JA conjugates containing small nonpolar amino acids also exhibit bioactivity but are much less abundant thanJA-Ile in plant tissues (75, 85, 165). Oxidized derivatives of JA-Ile, such as 12OH-JA-Ile, also retain partial activityin vitro (6, 84, 88). These data indicate that JA-Ile is the major ligand for the COI1–JAZ receptor system in higherplants but leave open the possibility that receptor activity is modulated through biochemical modification of JA-Ileor by coreceptor subtypes composed of particular COI1 and JAZ isoforms (165). Several studies have reportedCOI1-independent activities for various jasmonates, but their mechanism of action remains largely unknown (154).

coworkers (92) identified a jasmonate-inducible ABC transporter ( JAT1 or ABCG16) that, re-markably, mediates both the nuclear influx of JA-Ile and the cellular efflux of JA (Figure 4).Together with a growing list of other candidate JA transporters (112), these advances in under-standing the movement of endogenous jasmonates offer exciting new insights into the regulation ofsignaling, including the well-documented systemic effects of the hormone (44, 86). A key technicaladvance in this regard is the development of Jas motif–based fluorescent biosensors (e.g., Jas9-Venus) to map the spatiotemporal distribution of JA-Ile in healthy and stressed plant tissues (90).

De novo synthesis of stable JAZ proteins. Most JAZ genes are rapidly expressed in response tostresses that trigger JA-Ile accumulation and subsequent JAZ degradation (26, 30, 148, 168). If theresulting de novo synthesized JAZ repressors interact weakly or not at all with COI1 in the presenceof JA-Ile, they could reengage cognate transcription factors as a time-delay strategy to terminatesignaling (Figure 3). Analyses of Arabidopsis group IV JAZ proteins, including JAZ8 and JAZ13,support this hypothesis. These proteins harbor a noncanonical degron that interacts weakly withCOI1 and, as a consequence, enhances the protein’s stability and repressor activity in jasmonate-stimulated cells (137, 149). Accordingly, the ectopic expression of JAZ8 or JAZ13 resulted indecreased sensitivity to exogenous JA, a phenotype not observed upon ectopic expression of labileJAZ proteins that contain a canonical degron (26, 148, 168). These studies support the notion thatsequence variation in the JAZ degron provides a mechanism to respond to thresholds of JA-Ilethat are generated either spatially or temporally in plant tissues.

JAZ stability and repressor activity are also increased by alternative splicing events that truncateor completely remove the C-terminal Jas motif. Alternative splicing of JAZ10, for example, gen-erates three splice variants that either strongly ( JAZ10.1), weakly ( JAZ10.3), or fail to ( JAZ10.4)interact with COI1 in the presence of JA-Ile (Figure 2). These variants exhibit the expectedchanges in protein stability and repressive activity when overexpressed or mutated in planta (29,35, 108, 168). The alternative splicing event responsible for producing JAZ10.3 involves retaininga conserved intron (the so-called Jas intron) that is present in most JAZ genes from diverse landplants, including bryophytes (Figures 2 and 3) (28). Therefore, the retention of this intron duringpre-RNA splicing may represent a general mechanism for producing hyperstable JAZ proteins that


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strongly repress target transcription factors (174). JAZ-depleted mutants (18) generated by geneediting or other mutational approaches should provide important tools to further investigate therole of stable JAZ isoforms in the basal- and feedback-mediated repression of jasmonate responses.

Competing transcription factors. Another well-characterized mechanism for time-delayed ter-mination of MYC activity involves jasmonate-induced expression of a small group (bHLH subcladeIIId) of MYC-related DNA binding proteins, termed JASMONATE-ASSOCIATED MYC2-LIKE 1 ( JAM1), JAM2, and JAM3 (43, 111, 129, 140). Unlike MYCs, JAM proteins lack theability to activate transcription but retain DNA binding capacity. Thus, JAM proteins appear tocompete with MYC transcription factors for binding to cis-acting G-box elements in the promotersof jasmonate-responsive genes (Figure 3c). The ability of JAM proteins to bind JAZ via the con-served JID suggests that JAM activity is modulated by changes in the abundance of JAZ proteins,but further studies are needed to understand the functional relevance of JAM–JAZ complexes (43,140). It also remains to be determined whether negative feedback regulation by JAM proteinsoperates synergistically with, or independently of, newly synthesized, stable JAZ repressors orinduction of JA-Ile catabolic pathways. As mentioned above, multiple negative feedback loops areexpected to exhibit characteristic time delays to modulate the expression of specific sets of genes.It is likely that additional mechanisms to attenuate jasmonate signaling remain to be discovered,including rapid desensitization switches (e.g., posttranslational modification) that do not requirede novo protein synthesis.

Age-dependent decay of jasmonate signaling. Time-delay mechanisms to dampen jasmonateresponses also operate over longer developmental timescales. Mao and colleagues (102) showedthat the capacity of jasmonate signaling to induce anti-insect defense responses (e.g., inducibleglucosinolate biosynthesis) in Arabidopsis decays as leaves progress from juvenile to adult stage. Thisage-dependent attenuation of signaling is mediated by SQUAMOSA PROMOTER BINDINGPROTEIN-LIKE (SPL) transcription factors that directly bind to and stabilize JAZ, most likelyby interfering with SCFCOI1-mediated protein degradation. Thus, just as the induced expressionof stable JAZ proteins may attenuate signaling with a short time delay, JAZ stabilization viaSPL interaction provides a distinct mechanism to dampen defense responses with a longer time-delay signature. These findings have the potential to open up new areas of research to aid inunderstanding how and why patterns of defense change across plant ontogeny (8).

Organ- and Cell Type–Specific Modules

A key question concerning the regulation of jasmonate signaling is the extent to which organ-,tissue-, and cell type–specific modules contribute to the diversity and specificity of output re-sponses. Progress in addressing this issue has come from several directions. Characterization ofmutants exhibiting constitutive activation of a JAZ10 reporter gene showed that NINJA exertsmuch stronger corepressor activity in roots compared with aerial tissues (2). This highlights thepotential importance of NINJA-independent repression mechanisms in shoot tissues and paves theway for future work to understand organ specificity in JA-Ile signaling. Given the role of jasmonatesin stress-induced, long-distance signaling (44, 86), a related question is whether JA-Ile synthesis,perception, and subsequent transcription factor action occur in the same or different cell types.Results from organ-specific complementation experiments showed that hormone perception viaCOI1 in epidermal cells is sufficient to control aspects of anther function and pollen viability thatdepend on JA-Ile (69). These findings also suggest that a cell type–specific nonautonomous signalmay have a role in coordinating pollen maturation and anther dehiscence.


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Coronatine:a structural analog ofJA-Ile produced bysome virulent strainsof Pseudomonassyringae; also a potentagonist of COI1-JAZcoreceptors

The capacity of most JAZ proteins to interact with MYC2 (Figure 2), together with the paucityof jasmonate-related phenotypes in many jaz loss-of-function mutants, suggests a level of func-tional redundancy among members of the JAZ family (27). However, as spatial-specific expressionpatterns of individual JAZ genes are being revealed and studied in detail, this view of overlappingfunctions among JAZ proteins is being revised. In one example, guard cell–specific expression ofArabidopsis JAZ2 modulates stomatal behavior during infection with the bacterial pathogen Pseu-domonas syringae (50). This pathogen employs the JA-Ile mimic coronatine as a virulence factorto open stomata and gain entry to the plant apoplast (104). Coronatine-induced degradation ofJAZ2 derepresses MYC activity, which, in turn, activates downstream NAC transcription factors(ANAC19, ANAC55, and ANAC72) that inhibit salicylic acid production and promote stomatalopening (50). In a second example, expression profiling of JAZ genes in the ecological modelplant Nicotiana attenuata showed that one member of the family (JAZi ) is specifically expressed infloral tissues that contain high endogenous levels of JA and JA-Ile (93). JAZi belongs to the groupIV subfamily that includes the noncanonical JAZ13 in Arabidopsis (Figure 2) and, interestingly,interacts directly with a NINJA-like protein to repress MYC activity and restrain the productionof defense compounds in floral organs. These collective studies highlight the importance of cell-and organ-specific JAZ–transcription factor modules in controlling the specificity and diversity ofjasmonate responses.

THE INTEGRATION OF JASMONATE SIGNALINGAND MOLECULAR CROSSTALK

The discovery of JAZ proteins as transcriptional repressors of MYCs provided a conceptual frame-work to explain how fluctuating JA-Ile levels alter the expression of hormone-responsive targetgenes. Research during the past decade has revealed that JAZ proteins interact with many tran-scription factors other than MYCs to expand the range of jasmonate-regulated processes. Thefollowing section summarizes the state of knowledge of these multiple JAZ–transcription factormodules and discusses how this network contributes to the diversity and specificity of transcrip-tional outputs in the context of signal integration and molecular crosstalk.

JAZ Transcriptional Modules

Group III bHLH transcription factors serve broad roles in the plant life cycle and occupy a promi-nent role in the JAZ–transcription factor interaction network (50, 54) (Figure 5). As described pre-viously, the best characterized JAZ–transcription factor module comprises subgroup IIIe bHLHproteins that include MYC2, MYC3, MYC4, and MYC5. In many, if not most, plant species, JAZ–MYC transcriptional modules are particularly important for controlling the production of special-ized defense compounds, including those derived from alkaloid, terpenoid, phenylpropanoid, andamino acid biosynthetic pathways (54). MYC activity is further influenced by competition fromsubgroup IIId bHLH JAMs to attenuate MYC-dependent responses (Figure 3), as well as bycombinatorial interactions with other transcription factors. For example, MYC interaction withMYB transcription factors plays a crucial part in regulating the production of the glucosinolatesthat shape plant–herbivore relationships in the family Brassicaceae (133). MYCs also associatewith MYB21 and MYB24, which themselves interact with JAZ to control stamen and pollendevelopment in a tripartite JAZ–bHLH–MYB complex (Figure 5) (40, 54, 123, 141). AnotherJAZ–bHLH–MYB complex—consisting of the subgroup IIIf bHLH proteins ENHANCER OFGLABRA3 (EGL3), GLABRA3 (GL3), and TRANSPARENT TESTA GLABRA8 (TT8), andthe R2R3 MYBs MYB75 and GLABRA1 (GL1)—is involved in controlling trichome initiation and


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Figure 5JAZ interaction modules contribute to the diversity of jasmonate-regulated processes. (a) The JAZ interactome. JAZ-interactingproteins in the yellow sector modulate JAZ function by influencing protein stability [COI1 coreceptor, salicylic acid–associated NPRs(NPR3, NPR4)], through transcriptional repression (NINJA adaptor, TPL corepressor), or by interfering with protein–proteininteractions [the gibberellic acid–associated DELLAs (GAI, RGA, RGL1, RGL2, RGL3); aging-associated SPLs (SPL2, SPL9)].JAZ-interacting transcription factors shown in the blue sector execute jasmonate outputs and are colored according to transcriptionfactor family. Basic helix-loop-helix transcription factors ( green) have a prominent role in jasmonate signaling; MYCs (group IIIemembers MYC2, MYC3, MYC4, MYC5) control multiple outputs; JAMs (red; group IIId members JAM1, JAM2, JAM3) competitivelyantagonize MYCs; ICEs (group IIIb members ICE1, ICE2) work with MYCs to control cold tolerance; and EGLs (group IIIf membersEGL3, GL3, TT8) control an anthocyanin–trichome module with the MYB transcription factors ( gold; GL) GL1 and MYB75. MYCsalso interact with MYB subgroup 19 transcription factors (MYB21, MYB24, MYB57) to regulate flower development. Other JAZtranscription factor interactions involve YABs ( pink; FIL and YAB3) to modulate disease resistance and the production of anthocyaninsand chlorophyll; the EINs (blue; EIN3 and EIL1) to regulate ethylene responses; AP2 transcription factors ( purple; TOE1 and TOE2)to adjust flowering time; and a WRKY ( yellow; WRKY57), which participates in senescence. Arrows denote interactions that increaseJAZ repressor activity. Bars indicate negative regulation of transcription factor activity by JAZ or interactions that decrease JAZrepressor activity. (b) JAZ functional domains that interact with specific transcription factors (blue box) or other regulatory proteins thatdo not directly bind DNA ( yellow box). NT is the N-terminal region containing the CMID domain. (c) Examples of tripartiteprotein–protein interactions in which JAZ interacts with two partners that themselves interact. These three-way interactions appear tobe a common feature within the larger JAZ interaction network.

anthocyanin production (Figure 5) (54, 124, 125). That homologous JAZ–MYC–MYB complexesregulate anthocyanin biosynthesis in the epidermis of apple fruit (5) and fiber initiation in cotton(66) indicates that these JAZ–transcription factor modules are widespread in the plant kingdom.

In addition to myriad roles in biotic stress tolerance, several studies have demonstrated thatspecific JAZ–transcription factor modules control abiotic stress responses. In both Arabidopsisand banana, JAZ proteins interact with the subgroup IIIb bHLH proteins INDUCER OF CBFEXPRESSION 1 (ICE1) and ICE2 to promote cold acclimation responses (Figure 5) (67, 181).JAZ–bHLH transcription factor modules also control salt tolerance in rice. In this case, OsJAZ9interacts with OsbHLH062 to alter ion homeostasis, and the adaptor protein RICE SALTSENSITIVE3 (RSS3) links JAZ with bHLH proteins to reprogram root growth in high salinityenvironments (150, 159). These findings indicate that jasmonate signaling plays a greater part


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in abiotic stress responses than previously appreciated, and they raise interesting questions abouthow specific JAZ–transcription factor modules may be prioritized in response to multiple stressconditions.

The JAZ regulatory network extends beyond bHLH and MYB factors to include transcriptionfactors from several other families (Figure 5). JAZ interactions with the YABBY transcriptionfactors FILAMENTOUS FLOWER (FIL) and YAB3 contribute to jasmonate-mediated antho-cyanin accumulation, chlorophyll degradation, and disease resistance (11), whereas JAZ proteinsmodulate leaf senescence through direct interaction with WRKY57 (71). Jasmonate promotesdelayed flowering, in part, by modulating the activity of two JAZ-interacting AP2 transcriptionfactors, TARGET OF EAT1 (TOE1) and TOE2, which regulate expression of FLOWERINGLOCUS T (101, 173). JAZ interactions with ETHYLENE INSENSITIVE3 (EIN3) and EIN3-LIKE (EIL1) control jasmonate–ethylene synergism of root hair development and defense againstnecrotrophic pathogens, whereas MYC interaction with EIN3 or EIL1 antagonizes ethylene-mediated apical hook formation and jasmonate-mediated herbivore resistance (139, 179, 184). InArtemisia annua, JAZ interaction with a homeodomain leucine zipper (HD-ZIP) transcription fac-tor (AaHD1) regulates glandular trichome initiation and, consequently, the content of medicinalartemisinin in these structures (167). Collectively, these studies help to explain the diversity of JA-Ile-regulated responses across plant species and also highlight the modularity of JAZ–transcriptionfactor interactions.

The notion that JAZ proteins exert direct control over diverse transcription factors outsidethe MYC family is supported by genetic analyses showing that MYCs are required for many,but not all, JAZ-regulated traits in Arabidopsis (101). An important unanswered question concernsthe mechanisms by which JAZ proteins interact with and repress the activity of non-MYC tran-scriptional regulators; whereas MYCs bind to almost all JAZ proteins (Figure 2), most othertranscription factors interact with only a few JAZ (27). The Jas motif has been implicated in sev-eral of these non-MYC interactions (Figure 5b), but additional studies are needed to define themolecular and structural details of these associations.

JAZ Proteins As Nodes for Signal Crosstalk

JAZ proteins constitute a major hub for crosstalk with diverse stress and developmental signalingpathways that may serve to optimize plant fitness in changing environments (27, 53, 78, 142).These nodes of signal interaction modulate jasmonate signaling outputs by mechanisms tied tochanges in JAZ abundance or accessibility (Figure 5). For example, plant growth–defense bal-ance is controlled in part by JAZ–DELLA interactions that integrate JA-Ile and gibberellic acidsignaling, such that elevated gibberellic acid levels enhance JAZ repression of defense and, re-ciprocally, elevated JA-Ile levels enhance DELLA-mediated repression of growth (68, 142). In aseparate module involving jasmonate–gibberellic acid synergism, JAZ and DELLA proteins inter-act directly with and repress MYC2, GL3, EGL3, and GL1 to control sesquiterpene emission inflowers and trichome initiation in leaves (63, 124). JAZ proteins also integrate jasmonate signalingwith changes in light quality (i.e., shading) that signal the presence of plant competitors. Thisshade avoidance response is mainly controlled by the photoreceptor phytochrome B, and involveschanges in the abundance of DELLA, JAZ, and MYCs to favor growth over defense (24, 91).As alluded to above, JAZ repressor activity is also influenced by SPL transcription factors thatstabilize JAZ to attenuate jasmonate responsiveness during leaf development (102).

There is also progress in understanding how the core JA-Ile signaling pathway directly in-teracts with components of other stress hormone–response pathways. Examples of abscisic acid–jasmonate crosstalk include the E3 ubiquitin ligase KEEP ON GOING (KEG) that modulates


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JAZ12 stability (117), as well as the abscisic acid coreceptor PYL6 that interacts with and altersMYC2 transcriptional activity (3). Jasmonate-mediated antagonism of salicylic acid action stronglyinfluences plant immunity and is regulated by direct activation of ANAC transcription factors byMYC2, MYC3, and MYC4 (50, 182). Conversely, the salicylic acid receptors NPR3 and NPR4are implicated in the turnover of JAZ proteins as a potential mechanism to mount resistance tobiotrophic pathogens without compromising resistance to necrotrophic pathogens (96). There isalso evidence that the energy sensor SNF1-RELATED KINASE 1 (SnRK1) promotes JAZ desta-bilization to control sugar-induced anthocyanin accumulation (98). Collectively, these studieshighlight the importance of JAZ proteins as key nodes of crosstalk for integrating diverse signals.

Toward a Dynamic JAZ Interaction Network

Simplified models of jasmonate signaling typically depict a binary switch in which signaling iseither off or on in response to, respectively, low or high JA-Ile levels (Figure 3). In naturalenvironments, however, JA-Ile levels continuously fluctuate and are predicted by mathematicalmodels to exhibit pulse-like behavior (23, 86, 154). These considerations, together with the op-posing effects of JA-Ile on JAZ stability and induced JAZ expression, support the notion that JAZprotein levels are highly dynamic. The preponderance of predicted surface exposed and disor-dered regions outside the TIFY (ZIM) and Jas motifs (31; G.A. Howe, unpublished observations)further suggests that JAZ proteins have inherent structural flexibility to accommodate variouspartners that use different modes of binding, consistent with the high degree of connectivity be-tween JAZ proteins and other transcriptional regulators (Figure 5). Thus, fluctuating levels ofJA-Ile sensed by combinatorial assemblies of COI1–JAZ coreceptors not only may serve to alterthe transcriptional state of genes bound by JAZ–transcription factor complexes but also are likelyto mediate crosstalk between pathways by propagating changes in a broader protein–protein in-teraction network. For example, hormone-induced JAZ depletion relieves repression on MYCsand simultaneously allows DELLA proteins to bind and repress the activity of growth-promotingPHYTOCHROME-INTERACTING FACTOR transcription factors (PIFs) (169). In Arabidop-sis, JAZ degradation also promotes MYC heterodimerization with MYB transcription factors toactivate glucosinolate biosynthesis and anti-insect resistance (133).

A recurring but largely unexplained pattern of protein–protein interaction within the JAZ–transcription factor network involves two JAZ binding partners that physically interact with eachother (Figure 5c). Most prominent among these tripartite modules are transcriptional regulatorssuch as DELLA, MYB, EIN3, and ICE1, which interact with both JAZ and MYC2. These proteinsmay form ternary complexes in which JAZ impedes direct transcription factor–transcription factorinteraction until JA-Ile is perceived and JAZ degraded. Alternatively, two partners within thecircuit may compete with each other for binding to the third partner, as proposed for JAZ–DELLA interactions with cognate MYCs and PIFs (64, 169). Applying experimental approachesto interrogate the dynamics of protein assemblies that are scaffolded by JAZ will be useful forinvestigating the functional relevance of these interaction subnetworks.

THE MANIPULATION OF JASMONATE SIGNALINGBY PLANT-ASSOCIATED ORGANISMS

Many organisms whose life cycle is intimately associated with plants have evolved mechanismsthat co-opt or otherwise impair jasmonate signaling for their benefit. The nature of this manipu-lation typically depends on the type of host immunity encountered by the invading organism. Ingeneral, biotrophic and hemibiotrophic pathogens that elicit salicylic acid–dependent immunity


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JA-Ile C18:3 JA-mediated

defense

SAP11,Abm MiSSP7 βC1JA-Ile,

CFA-Ile, CORHopZ1a,

AvrB HopX1 HopBB1

Receptor ligands Repressor stability MYC activity

Activators

Suppressors

JAZ MYCCOI1

Figure 6Plant-interacting organisms deploy effectors that target the core jasmonate pathway to circumvent host plant immunity. Effectorseither activate JA-Ile signaling (blue) to antagonize salicylic acid–mediated plant immunity or interfere with and suppress JA-Ilesignaling (red ). Some organisms deplete host JA-Ile pools by decreasing JA biosynthesis (SAP11) or by catalyzing 12-hydroxylation ofJA (Abm). Other pathogens stimulate the signaling pathway by producing JA-Ile or coronafacoyl phytotoxins [such as CFA-Ile andcoronatine (COR)] that are agonists of the COI1–JAZ coreceptor. JAZ stability is modulated by effectors that promote (HopZ1a, AvrB)or interfere (MiSSP7) with COI1–JAZ interaction (and subsequent JAZ degradation), or by effectors that degrade JAZ proteins(HopX1). MYC activity is affected by interference with JAZ-mediated repression of MYCs (HopBB1) and by disrupting MYCactivation of jasmonate responses (βC1).

deploy effectors that activate jasmonate signaling to antagonize salicylic acid action. Conversely,necrotrophic parasites and herbivores that trigger jasmonate defenses employ mechanisms thatsuppress this branch of immunity. As knowledge of immune signaling networks has matured, it isbecoming increasingly clear that core components of the JA-Ile signaling pathway are a frequenttarget of diverse pathogen effectors (Figure 6) (51, 53, 77, 163, 177). This convergence of multiplevirulence factors on a major hub of the plant immune system provides compelling evidence for theimportance of jasmonate in mediating plant interactions with associated biota, and also highlightskey control points in the JA-Ile signaling pathway.

Pathogen Effectors As Receptor Ligands

As illustrated by the phytotoxin coronatine, which is synthesized by some plant pathogenic strainsof Pseudomonas syringae, an effective strategy to suppress salicylic acid–based immunity amonghemi- and biotrophic bacterial pathogens is the secretion of structural analogs of JA-Ile thatactivate the COI1–JAZ receptor system (47, 75, 135). The existence of distinct pathways forthe biosynthesis of coronatine and related coronafacoyl phytotoxins, including the Ile conjugateof coronafacic acid (Figure 4) (165), supports the notion that the JA-Ile signaling pathway is aconvergent target of these pathogens (17). This strategy for suppressing host immunity extendsto fungal pathogens as well. For example, many pathogenic and saprophytic fungi produce largequantities of naturally active isomers of JA and JA-Ile, which appears to be a critical factor forpathogenicity (32, 51, 53). Collectively, these findings indicate that the production of bioactivejasmonates or their precursors by pathogens represents a general strategy to antagonize the salicylicacid–dependent sector of plant immunity. Research aimed at understanding the biosynthesis of JA,JA-Ile, and JA-Ile mimics (e.g., coronafacoyl phytotoxins) by plant pathogens promises to providea fascinating window into coevolving molecular processes that shape these biotic interactions (13,113).

Some plant-associated organisms deploy effectors that interfere with the ability of the hostto produce JA-Ile (Figure 6). The phytoplasma Aster yellows, which is transmitted by insectleafhoppers, suppresses JA-Ile-dependent defenses to improve the performance of its insectvector (146). The Aster yellows effector SAP11 destabilizes the transcriptional activators ofthe JA biosynthetic gene LOX2 and decreases JA-Ile levels to bolster leafhopper survival andfecundity (146). Other effectors interfere with host JA-Ile production by metabolizing precursors


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of the hormone. Rice blast fungus (Magnaporthe oryzae) secretes a monooxygenase (Abm) thatcatabolizes JA to suppress JA-Ile-mediated immunity in rice (114). This mode of virulence iscomparable to the role of plant JA oxidases ( JOXs and JAOs) in attenuating JA-Ile signaling byconverting JA to 12OH-JA (Figure 4) (15, 138). Several other examples of JA catabolism byplant-associated fungi suggest that perturbation of JA-Ile biosynthesis is a common mechanismfor enhancing the virulence of plant pathogens (106).

Effectors that Modify JAZ Stability

Microbial effectors also manipulate JAZ stability, either by influencing COI1–JAZ interactionsor by direct proteolysis (Figure 6). The P. syringae effectors HopZ1a and AvrB both enhanceCOI1-mediated degradation of JAZ proteins. HopZ1a acetylates JAZ proteins to target them fordegradation by the SCFCOI1-proteasome pathway, resulting in suppression of stomatal immu-nity (70, 99). In addition to other effector functions, AvrB promotes COI1–JAZ interaction andJAZ degradation by an unknown mechanism involving elevated activity of a plasma membraneproton ATPase (183). The P. syringae effector HopX1 is a cysteine protease that degrades JAZproteins independently of SCFCOI1 (49). By contrast, the fungal mutualist Laccaria bicolor sup-presses jasmonate-regulated defenses to permit colonization of its host. This is achieved throughdeployment of the MiSSP7 effector, which interacts with and stabilizes a JAZ protein against JA-Ile-mediated degradation (120). Consistent with the concept of JAZ proteins as common targetsfor pathogen hijacking, large-scale, protein–protein interaction screens of effectors from bacterial,fungal, and oomycete biotrophs have revealed JAZ3 as a cross-kingdom target of effectors (110,155).

Effectors that Interfere with MYC Transcription Factors

Some effectors also modulate the activity of jasmonate-regulated transcription factors, includingMYCs. HopBB1 from P. syringae manipulates JAZ proteins to activate JA-Ile signaling and suppressplant immunity. One effector function of HopBB1 is to interfere with JAZ–MYC interactions torelease MYCs from repression (170). Begomovirus, which is transmitted by whiteflies, uses the βC1effector to disrupt terpene-based plant defenses and enhance the performance of its insect vector(94). The βC1 effector interacts with MYC2, which disrupts the activation of MYC-regulatedterpene synthases and reduces whitefly resistance (94). The broad-spectrum nature of JA-Ile-triggered immunity implies that additional mechanisms to manipulate JA-Ile signaling by plant-associated organisms remain to be discovered, including those that operate across multitrophiclevels (1).

THE EVOLUTION OF JASMONATE SIGNALING

Based on the observation that genes encoding putative components of the core JA-Ile responsepathway are present in early land plants but not aquatic green algae (152), it is generally as-sumed that hormonally active jasmonates evolved in response to selective conditions associatedwith plant colonization of land approximately 450 Mya. Nevertheless, accurate tracing of theevolutionary history of this lipid-based signaling system requires functional studies with speciesin representative phylogenetic groups, particularly in the basal lineages of extant land plants.There is compelling experimental evidence that JA-Ile synthesis and signaling is conserved inboth seedless and seed-bearing vascular plants (122). However, less certain is the extent to whichthe pathway operates in ancient nonvascular plants, such as the model moss Physcomitrella patens


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and liverwort, M. polymorpha. At least some species within these bryophyte lineages have enzy-matic capacity to produce the C18 JA precursor 12-oxo-phytodienoic acid (OPDA) but, owingto the absence of OPR3 (OPDA reductase) and JAR1, do not appear to synthesize JA or JA-Ile(12, 121, 145, 162, but also see Reference 171). There is evidence that OPDA promotes the well-known developmental functions of jasmonates in P. patens and M. polymorpha, including fertilityand growth inhibition (145, 162). That OPDA levels are elevated in M. polymorpha in responseto mechanical tissue damage further suggests that stress-induced formation of C18 pentacyclicoxylipins may represent an ancestral stress response (162), which was followed by the emergenceof JA and JA-Ile biosynthetic capacity in early vascular plants (122). The presence in bryophytesof putative COI1 and JAZ homologs (12, 152) has raised the intriguing possibility that the activeform of the hormone in ancient land plants may be OPDA or an OPDA derivative other thanJA or JA-Ile (14). The presence of a canonical degron sequence in bryophyte JAZ proteins (e.g.,M. polymorpha JAZ) (Figure 2) is not necessarily at odds with this hypothesis if, for example, mod-ifications in the cognate COI1 coreceptor accommodated a ligand other than JA-Ile (135). Func-tional analyses of the COI1–JAZ–transcription factor module in bryophyte lineages are clearlywarranted for the insights they will provide into the early origins and physiological functions ofthe pathway.

The discovery that COI1 is homologous to TIR1 and related F-box proteins that mediateauxin perception was the first of many telltale signs that the regulatory logic of JA-Ile signal-ing has striking parallels to the auxin response pathway (34, 59, 74, 118, 161). Nevertheless, theextent to which JA-Ile and auxin signaling share a common ancestry may be limited to COI1and TIR1, which appear to have evolved in land plants from an ancestral algal gene that en-codes an F-box protein lacking key residues for perceiving these hormones (12). The lack ofsequence similarity between JAZ repressors and Aux/IAA repressors and their cognate transcrip-tion factor targets [(respectively, MYCs and Auxin Response Factors (ARFs)] supports a scenarioin which COI1 and TIR1 diversified following duplication and neofunctionalization of an an-cestral land plant F-box gene, but in which the JAZ–MYC and Aux/IAA–ARF modules aroseindependently of each other. For example, it is conceivable that JAZ repressors evolved from anancestral TIFY protein in response to selective pressure to mitigate the high cost of constitu-tively expressed defense traits under the control of MYCs (57). The subsequent emergence ofCOI1 and its associated ancient ligand would reflect a major step in the evolution of inducedresistance because it provided a mechanism to couple stress perception to oxylipin synthesis andderepression of appropriate defense-related genes (57). Although this hypothesis implies that theevolution of jasmonate signaling was driven by the selective advantages conferred by stress toler-ance, an ancestral function for the hormone in growth or other developmental processes cannot beexcluded.

TRANSLATIONAL APPLICATIONS IN JASMONATE RESEARCH

The central role of jasmonates in plant resilience to environmental stress has long been an attractivebiotechnological target for researchers (153). Detailed knowledge of JA-Ile signaling opens upexciting opportunities for translational research to reduce crop losses resulting from environmentalstress and also to harness the cornucopia of valuable plant products whose biosynthesis is controlledby JAZ–transcription factor modules. Here, we highlight present and potential future researchdirections aimed at engineering the core JA-Ile signaling pathway for desirable plant traits.

It is well established that jasmonates exert master control over an immense reservoir of plantbiosynthetic pathways that produce natural pesticides and other specialized metabolites (48).Considerable attention has focused on medicinally important jasmonate-regulated metabolites,


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including the antimalarial agent artemisinin and the anticancer drugs vinblastine and paclitaxel.Several studies also implicate jasmonate signaling in the control of metabolic gene clusters thatspecify the production of triterpenoids and other important plant metabolites (45, 101). JA elicita-tion experiments provide a powerful approach to mining coexpressed biosynthetic genes in specificpathways that are often silent in the absence of stress; this approach has also proved useful foridentifying candidate transcription factors that control these pathways (54). Beyond coexpressionstudies, constitutive activation of JA-Ile signaling can be used to enhance the production of spe-cialized metabolites and resistance to biotic aggressors. Genetic strategies to achieve this includeactivating upstream elicitors of JA synthesis (21, 36), jaz mutations that relieve repression on tran-scription factors (18, 147), and genetic strategies to mitigate negative feedback loops (61, 83). In thecase of pathways governed by MYCs, the engineering of these transcription factors for insensitivityto JAZ repression offers a particularly promising approach to enhancing the expression of path-ways in a targeted manner and independently of JA-Ile levels (45, 55). Gaining structural insights(174, 175) into the mechanism of JAZ-mediated transcriptional repression will facilitate suchefforts.

Indeed, several studies have exploited the structural knowledge of the COI1–JAZ coreceptorcomplex (135) to alter the physiological outcomes of hormone signaling to enhance plant resis-tance to pathogens. Zhang et al. (176) used a systematic mutagenesis approach to identify a singleamino acid substitution in the ligand binding pocket of COI1 that accommodates endogenousJA-Ile but not the phytotoxic agonist coronatine. Arabidopsis plants expressing this modified re-ceptor maintained robust resistance to insect herbivores whose feeding elicits JA-Ile production,but were more resistant to infection by coronatine-producing strains of P. syringae. This approachis significant in establishing the proof of concept that host resistance can be broadened by mod-ifying the targets of pathogen effectors without compromising resistance to other types of plantenemies. Monte et al. (107) showed that a synthetic ligand, coronatine-O-methyloxime, compet-itively antagonizes COI1–JAZ coreceptor activity to potentiate resistance to P. syringae strainsthat produce coronatine. These structure-guided approaches for modifying ligand–receptor in-teraction may ultimately be used to repurpose existing coreceptor modules for enhanced chemicalcontrol of crop resistance and to design novel coreceptor subtypes that selectively control desiredtranscriptional outputs.

A significant barrier to using jasmonates for crop protection is that activation of the pathwayis often associated with reductions in plant growth and fitness (57, 60, 168, 180). Several stud-ies provide proof of principle that such growth–defense trade-offs can be uncoupled to allow forsimultaneous defense and growth, at least under controlled laboratory conditions. Genetic uncou-pling of jasmonate-mediated growth–defense trade-offs in Arabidopsis was achieved by inactivatingphytochrome B in a genetic background lacking five JAZ repressors (18). Rewiring defense- andlight-signaling pathways in this manner may provide a strategy for cultivating densely planted cropswith less dependence on pesticides. Remarkably, treating plants with macrolactone derivatives ofJA-Ile was shown to activate defense responses in N. attenuata without reducing growth or fitness(72). Although additional research is needed to determine whether JA-Ile macrolactones exertthese effects through the COI1–JAZ receptor system, this finding raises the possibility of boost-ing crop yield and stress resilience via the application of small molecules that selectively activatedefense traits without impeding growth. Studies in rice demonstrate that JAZ overexpression isalso a viable strategy for increasing grain yield and biomass, even at the elevated temperatures thatreduce the yield of wild-type plants (58). As our mechanistic understanding of JAZ–transcriptionfactor interactions increases, the use of engineered JAZ scaffolds may accelerate the rational designof jasmonate signaling for improved crop performance.


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SUMMARY POINTS

1. The core JA-Ile signaling pathway consists of functional modules for transcription factorrepression, JAZ degradation, and transcriptional activation. MYCs have a dominant rolein mediating jasmonate responses, but many other JAZ-interacting transcription factorscontribute to the complexity and specificity of signaling outputs.

2. A JA-Ile-induced conformational change in the Jas α-helix is a key part of the molecularswitch that converts MYCs from repressors to transcriptional activators. This off/onswitch depends on JAZ degradation, and it involves the dissociation of corepressors andrecruitment of coactivators, including Mediator.

3. The core signaling pathway is subject to multiple levels of negative feedback control thatlikely operate with a characteristic time delay to tailor spatial and temporal terminationof jasmonate responses.

4. Whereas the core JA-Ile signaling pathway is highly conserved in land plants, inductiveinput signals and physiological responses are highly diverse. This level of response di-versity may help explain the idiosyncratic distribution of specialized metabolites in theplant kingdom, and it highlights the evolution of JAZ–transcription factor modules as akey step in the diversification of jasmonate responses.

5. The major role of JA-Ile in plant immunity is highlighted by the plethora of pathogensthat use effectors to manipulate JA-Ile biosynthesis or action. In addition to biotic stressresilience, increasing evidence supports a key role for the hormone in plant responses todrought, salt, temperature extremes, and other abiotic stresses.

6. JAZ proteins are a major hub for molecular crosstalk and the integration of jasmonatewith other signaling pathways.

7. The core JA-Ile signaling pathway appears to be conserved in all vascular plants, butmore research is needed to understand jasmonate perception and signaling systems inbryophyte lineages.

8. The present mechanistic insights into JA-Ile signaling will accelerate practical applica-tions for improving the stress tolerance of crops, and for achieving sustainable productionof valuable plant-derived compounds whose synthesis is controlled by this hormone.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

We thank the many colleagues who have contributed to jasmonate research and apologize tothose whose work was not included owing to space limitations. Jasmonate research in G.A.H.’slaboratory is supported by grants from the Chemical Sciences, Geosciences and Biosciences Di-vision, Basic Energy Sciences, Office of Science at the US Department of Energy through grantDE-FG02–91ER20021; the National Institutes of Health through grant R01GM57795; and theNational Science Foundation through grant IOS-1456864. G.A.H. also acknowledges supportfrom the Michigan AgBioResearch Project through grant MICL02278. Jasmonate research in


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A.J.K.’s laboratory is supported by the National Science Foundation (IOS-1557439) and the Foodfor the 21st Century program at the University of Missouri.

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138. Smirnova E, Marquis V, Poirier L, Aubert Y, Zumsteg J, et al. 2017. Jasmonic acid oxidase 2 ( JAO2)hydroxylates jasmonic acid and represses basal defense and resistance responses against Botrytis cinereainfection. Mol. Plant 10:115973

139. Song S, Huang H, Gao H, Wang J, Wu D, et al. 2014. Interaction between MYC2 and ETHYLENEINSENSITIVE3 modulates antagonism between jasmonate and ethylene signaling in Arabidopsis. PlantCell 26:263–79

140. Song S, Qi T, Fan M, Zhang X, Gao H, et al. 2013. The bHLH subgroup IIId factors negatively regulatejasmonate-mediated plant defense and development. PLOS Genet. 9:e1003653


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141. Song S, Qi T, Huang H, Ren Q, Wu D, et al. 2011. The jasmonate-ZIM domain proteins interactwith the R2R3-MYB transcription factors MYB21 and MYB24 to affect jasmonate-regulated stamendevelopment in Arabidopsis. Plant Cell 23:1000–13

142. Song S, Qi T, Wasternack C, Xie D. 2014. Jasmonate signaling and crosstalk with gibberellin andethylene. Curr. Opin. Plant Biol. 21:112–19

143. This and otherwork on the JAR1conjugating enzymedemonstrate that JA-Ileis an active form of thehormone.

143. Staswick PE, Tiryaki I. 2004. The oxylipin signal jasmonic acid is activated by an enzyme thatconjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–27

144. Stitz M, Baldwin IT, Gaquerel E. 2011. Diverting the flux of the JA pathway in Nicotiana attenuatacompromises the plant’s defense metabolism and fitness in nature and glasshouse. PLOS ONE 6:e25925

145. Stumpe M, Gobel C, Faltin B, Beike AK, Hause B, et al. 2010. The moss Physcomitrella patens containscyclopentenones but no jasmonates: Mutations in allene oxide cyclase lead to reduced fertility and alteredsporophyte morphology. New Phytol. 188:740–49

146. Sugio A, Kingdom HN, MacLean AM, Grieve VM, Hogenhout SA. 2011. Phytoplasma protein effectorSAP11 enhances insect vector reproduction by manipulating plant development and defense hormonebiosynthesis. PNAS 108:E1254–63

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148. Describes thediscovery of JAZproteins; shows thatJA-Ile is the ligand thatpromotes COI1-JAZinteraction (also see 26,168).

148. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, et al. 2007. JAZ repressor proteins aretargets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–65

149. Thireault C, Shyu C, Yoshida Y, St. Aubin B, Campos ML, Howe GA. 2015. Repression of jasmonatesignaling by a non-TIFY JAZ protein in Arabidopsis. Plant J. 82:669–79

150. Toda Y, Tanaka M, Ogawa D, Kurata K, Kurotani K-I, et al. 2013. RICE SALT SENSITIVE3 forms aternary complex with JAZ and class-C bHLH factors and regulates jasmonate-induced gene expressionand root cell elongation. Plant Cell 25:1709–25

151. Vanholme B, Grunewald W, Bateman A, Kohchi T, Gheysen G. 2007. The tify family previously knownas ZIM. Trends Plant Sci. 12:239–44

152. Wang C, Liu Y, Li SS, Han GZ. 2015. Insights into the origin and evolution of plant hormone signalingmachinery. Plant Physiol. 167:872–886

153. Wasternack C. 2014. Action of jasmonates in plant stress responses and development—applied aspects.Biotechnol. Adv. 32:31–39

154. Wasternack C, Hause B. 2013. Jasmonates: biosynthesis, perception, signal transduction and action inplant stress response, growth and development: an update to the 2007 review in Annals of Botany. Ann.Bot. 111:1021–58

155. Wessling R, Epple P, Altmann S, He Y, Yang L, et al. 2014. Convergent targeting of a common hostprotein-network by pathogen effectors from three kingdoms of life. Cell Host Microbe 16:364–75

156. Widemann E, Miesch L, Lugan R, Holder E, Heinrich C, et al. 2013. The amidohydrolases IAR3 andILL6 contribute to jasmonoyl-isoleucine hormone turnover and generate 12-hydroxyjasmonic acid uponwounding in Arabidopsis leaves. J. Biol. Chem. 288:31701–14

157. Withers J, Yao J, Mecey C, Howe GA, Melotto M, He SY. 2012. Transcription factor-dependent nuclearlocalization of a transcriptional repressor in jasmonate hormone signaling. PNAS 109:20148–53

158. Woldemariam MG, Onkokesung N, Baldwin IT, Galis I. 2012. Jasmonoyl-L-isoleucine hydrolase 1( JIH1) regulates jasmonoyl-L-isoleucine levels and attenuates plant defenses against herbivores. Plant J.72:758–67

159. Wu H, Ye H, Yao R, Zhang T, Xiong L. 2015. OsJAZ9 acts as a transcriptional regulator in jasmonatesignaling and modulates salt stress tolerance in rice. Plant Sci. 232:1–12

160. Wu K, Zhang L, Zhou C, Yu CW, Chaikam V. 2008. HDA6 is required for jasmonate response,senescence and flowering in Arabidopsis. J. Exp. Bot. 59:225–34

161. Identifies COI1 asan F-box protein andimplicatesubiquitination in thejasmonate responsepathway.

161. Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG. 1998. COI1: an Arabidopsis gene requiredfor jasmonate-regulated defense and fertility. Science 280:1091–94

162. Yamamoto Y, Ohshika J, Takahashi T, Ishizaki K, Kohchi T, et al. 2015. Functional analysis of alleneoxide cyclase, MpAOC, in the liverwort Marchantia polymorpha. Phytochemistry 116:48–56


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163. Yan C, Xie D. 2015. Jasmonate in plant defence: sentinel or double agent? Plant Biotechnol. J. 13:1233–40164. Yan J, Li H, Li S, Yao R, Deng H, et al. 2013. The Arabidopsis F-box protein CORONATINE INSEN-

SITIVE1 is stabilized by SCFCOI1 and degraded via the 26S proteasome pathway. Plant Cell 25:486–98165. Yan J, Li S, Gu M, Yao R, Li Y, et al. 2016. Endogenous bioactive jasmonate is composed of a set of

(+)-7-iso-JA-amino acid conjugates. Plant Physiol. 172:2154–64166. Yan J, Zhang C, Gu M, Bai Z, Zhang W, et al. 2009. The Arabidopsis CORONATINE INSENSITIVE1

protein is a jasmonate receptor. Plant Cell 21:2220–36167. Yan T, Chen M, Shen Q, Li L, Fu X, et al. 2017. HOMEODOMAIN PROTEIN 1 is required for

jasmonate-mediated glandular trichome initiation in Artemisia annua. New Phytol. 213:1145–55168. Describes thediscovery of JAZproteins (also see 26,148).

168. Yan Y, Stolz S, Chetelat A, Reymond P, Pagni M, et al. 2007. A downstream mediator in thegrowth repression limb of the jasmonate pathway. Plant Cell 19:2470–83

169. Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ, et al. 2012. Plant hormone jasmonate prioritizes defenseover growth by interfering with gibberellin signaling cascade. PNAS 109:1192–200

170. Yang L, Teixeira PJ, Biswas S, Finkel OM, He Y, et al. 2017. Pseudomonas syringae type III effectorHopBB1 promotes host transcriptional repressor degradation to regulate phytohormone responses andvirulence. Cell Host Microbe 21:156–68

171. Zaveska Drabkova L, Dobrev PI, Motyka V. 2015. Phytohormone profiling across the bryophytes. PLOSONE 10:e0125411

172. Zhai Q, Yan L, Tan D, Chen R, Sun J, et al. 2013. Phosphorylation-coupled proteolysis of the tran-scription factor MYC2 is important for jasmonate-signaled plant immunity. PLOS Genet. 9:e1003422

173. Zhai Q, Zhang X, Wu F, Feng H, Deng L, et al. 2015. Transcriptional mechanism of jasmonate receptorCOI1-mediated delay of flowering time in Arabidopsis. Plant Cell 27:2814–28

174. Zhang F, Ke J, Zhang L, Chen R, Sugimoto K, et al. 2017. Structural insights into alternative splicing–mediated desensitization of jasmonate signaling. PNAS 114:1720–25

175. Reports the X-raycrystal structure of theMYC3-JAZ9 complexand shows that JAZ andMED25 compete forMYC3 binding.

175. Zhang F, Yao J, Ke J, Zhang L, Lam VQ, et al. 2015. Structural basis of JAZ repression of MYCtranscription factors in jasmonate signalling. Nature 525:269–73

176. Zhang L, Yao J, Withers J, Xin XF, Banerjee R, et al. 2015. Host target modification as a strategy tocounter pathogen hijacking of the jasmonate hormone receptor. PNAS 112:14354–59

177. Zhang L, Zhang F, Melotto M, Yao J, He SY. 2017. Jasmonate signaling and manipulation by pathogensand insects. J. Exp. Bot. 68:1371–85

178. Zhang T, Poudel AN, Jewell JB, Kitaoka N, Staswick P, et al. 2016. Hormone crosstalk in woundstress response: Wound-inducible amidohydrolases can simultaneously regulate jasmonate and auxinhomeostasis in Arabidopsis thaliana. J. Exp. Bot. 67:2107–20

179. Zhang X, Zhu Z, An F, Hao D, Li P, et al. 2014. Jasmonate-activated MYC2 represses ETHYLENEINSENSITIVE3 activity to antagonize ethylene-promoted apical hook formation in Arabidopsis. PlantCell 26:1105–17

180. Zhang Y, Turner J. 2008. Wound-induced endogenous jasmonates stunt plant growth by inhibitingmitosis. PLOS ONE 3:e3699

181. Zhao M-L, Wang J-N, Shan W, Fan J-G, Kuang J-F, et al. 2013. Induction of jasmonate signallingregulators MaMYC2s and their physical interactions with MaICE1 in methyl jasmonate-induced chillingtolerance in banana fruit. Plant Cell Environ. 36:30–51

182. Zheng XY, Spivey NW, Zeng W, Liu PP, Fu ZQ, et al. 2012. Coronatine promotes Pseudomonas syringaevirulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell HostMicrobe 11:587–96

183. Zhou Z, Wu Y, Yang Y, Du M, Zhang X, et al. 2015. An Arabidopsis plasma membrane proton ATPasemodulates JA signaling and is exploited by the Pseudomonas syringae effector protein AvrB for stomatalinvasion. Plant Cell 27:2032–41

184. Zhu Z, An F, Feng Y, Li P, Xue L, et al. 2011. Derepression of ethylene-stabilized transcription factors(EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. PNAS 108:12539–44

185. Zust T, Agrawal AA. 2017. Trade-offs between plant growth and defense: an emerging mechanisticsynthesis. Annu. Rev. Plant Biol. 68:513–34


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PP69_FrontMatter ARI 5 April 2018 9:11

Annual Review ofPlant Biology

Volume 69, 2018

Contents

My Secret LifeMary-Dell Chilton � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Diversity of Chlorophototrophic Bacteria Revealed in the Omics EraVera Thiel, Marcus Tank, and Donald A. Bryant � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �21

Genomics-Informed Insights into Endosymbiotic Organelle Evolutionin Photosynthetic EukaryotesEva C.M. Nowack and Andreas P.M. Weber � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �51

Nitrate Transport, Signaling, and Use EfficiencyYa-Yun Wang, Yu-Hsuan Cheng, Kuo-En Chen, and Yi-Fang Tsay � � � � � � � � � � � � � � � � � � � � �85

Plant VacuolesTomoo Shimada, Junpei Takagi, Takuji Ichino, Makoto Shirakawa,

and Ikuko Hara-Nishimura � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 123

Protein Quality Control in the Endoplasmic Reticulum of PlantsRichard Strasser � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 147

Autophagy: The Master of Bulk and Selective RecyclingRichard S. Marshall and Richard D. Vierstra � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 173

Reactive Oxygen Species in Plant SignalingCezary Waszczak, Melanie Carmody, and Jaakko Kangasjarvi � � � � � � � � � � � � � � � � � � � � � � � � � � 209

Cell and Developmental Biology of Plant Mitogen-Activated ProteinKinasesGeorge Komis, Olga Samajova, Miroslav Ovecka, and Jozef Samaj � � � � � � � � � � � � � � � � � � � � � 237

Receptor-Like Cytoplasmic Kinases: Central Players in Plant ReceptorKinase–Mediated SignalingXiangxiu Liang and Jian-Min Zhou � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 267

Plant Malectin-Like Receptor Kinases: From Cell Wall Integrity toImmunity and BeyondChristina Maria Franck, Jens Westermann, and Aurelien Boisson-Dernier � � � � � � � � � � � � 301

Kinesins and Myosins: Molecular Motors that Coordinate CellularFunctions in PlantsAndreas Nebenfuhr and Ram Dixit � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 329

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The Oxylipin Pathways: Biochemistry and FunctionClaus Wasternack and Ivo Feussner � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 363

Modularity in Jasmonate Signaling for Multistress ResilienceGregg A. Howe, Ian T. Major, and Abraham J. Koo � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 387

Essential Roles of Local Auxin Biosynthesis in Plant Developmentand in Adaptation to Environmental ChangesYunde Zhao � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 417

Genetic Regulation of Shoot ArchitectureBing Wang, Steven M. Smith, and Jiayang Li � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 437

Heterogeneity and Robustness in Plant Morphogenesis: From Cellsto OrgansLilan Hong, Mathilde Dumond, Mingyuan Zhu, Satoru Tsugawa,

Chun-Biu Li, Arezki Boudaoud, Olivier Hamant, and Adrienne H.K. Roeder � � � � � � 469

Genetically Encoded Biosensors in Plants: Pathways to DiscoveryAnkit Walia, Rainer Waadt, and Alexander M. Jones � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 497

Exploring the Spatiotemporal Organization of Membrane Proteins inLiving Plant CellsLi Wang, Yiqun Xue, Jingjing Xing, Kai Song, and Jinxing Lin � � � � � � � � � � � � � � � � � � � � � � � 525

One Hundred Ways to Invent the Sexes: Theoretical and ObservedPaths to Dioecy in PlantsIsabelle M. Henry, Takashi Akagi, Ryutaro Tao, and Luca Comai � � � � � � � � � � � � � � � � � � � � � � 553

Meiotic Recombination: Mixing It Up in PlantsYingxiang Wang and Gregory P. Copenhaver � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 577

Population Genomics of Herbicide Resistance: Adaptation viaEvolutionary RescueJulia M. Kreiner, John R. Stinchcombe, and Stephen I. Wright � � � � � � � � � � � � � � � � � � � � � � � � � 611

Strategies for Enhanced Crop Resistance to Insect PestsAngela E. Douglas � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 637

Preadaptation and Naturalization of Nonnative Species: Darwin’s TwoFundamental Insights into Species InvasionMarc W. Cadotte, Sara E. Campbell, Shao-peng Li, Darwin S. Sodhi,

and Nicholas E. Mandrak � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 661

Macroevolutionary Patterns of Flowering Plant Speciationand ExtinctionJana C. Vamosi, Susana Magallon, Itay Mayrose, Sarah P. Otto,

and Herve Sauquet � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 685

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When Two Rights Make a Wrong: The Evolutionary Genetics ofPlant Hybrid IncompatibilitiesLila Fishman and Andrea L. Sweigart � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 707

The Physiological Basis of Drought Tolerance in Crop Plants:A Scenario-Dependent Probabilistic ApproachFrancois Tardieu, Thierry Simonneau, and Bertrand Muller � � � � � � � � � � � � � � � � � � � � � � � � � � � � 733

Paleobotany and Global Change: Important Lessons for Species toBiomes from Vegetation Responses to Past Global ChangeJennifer C. McElwain � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 761

Trends in Global Agricultural Land Use: Implications forEnvironmental Health and Food SecurityNavin Ramankutty, Zia Mehrabi, Katharina Waha, Larissa Jarvis,

Claire Kremen, Mario Herrero, and Loren H. Rieseberg � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 789

Errata

An online log of corrections to Annual Review of Plant Biology articles may be found athttp://www.annualreviews.org/errata/arplant

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Documents

Modularity in Jasmonate Signaling for Multistress Resilience