5

Jasmonates in Stress, Growth, and Development

Claus Wasternack

5.1

Introduction

In contrast to animals, plants are under continuous pressure to adapt to fluctua-

tions in the environment. Apart from the essential factors of light, water, and

nutrients, they have to monitor other abiotic factors such as oxygen, salt, gravity,

touch, osmotic pressure, temperature, and chemicals. For unfavorable levels of

these factors, plants have developed a reprogramming of gene expression leading to

adaption to such stress conditions. Similar dramatic reprogramming of plant gene

expression takes place upon biotic stress by pathogenic microorganisms, by her-

bivorous insects, or symbiotic interactions such as arbuscular mycorrhiza. Each of

these interactions and adaptations is based on a complex signaling network of

convergent and divergent signaling pathways. In addition to other plant hormones,

such as ethylene (ET), abscisic acid (ABA), cytokinins, and auxins, jasmonic acid

(JA) and its derivatives are important signals in plant stress responses. JA and its

metabolites such as JA methyl ester (jasmonic acid methyl ester JAME) and amino

acid conjugates, commonly named jasmonates, are lipid-derived signals. In the last

two decades, most of them including the JA precursor 12-oxo-phytodienoic acid

(OPDA) were recognized as being components of an at least partially occurring

intracellular, intercellular, systemic as well as interorganismal signal transduction

in response to biotic and abiotic stress.

However, many developmental processes are also known in which jasmonates

function as an essential signal. Among them are germination and root growth,

senescence, tuberization, and some stages of flower development.

Over the last two decades, there has been a steady increase in publications on

jasmonates. Consequently, reviews have appeared continuously covering different

aspects of JA biosynthesis, action and signal transduction (e.g., since 2005: [1–12]).

This chapter will discuss recent results on some aspects of the biosynthesis,

metabolism and action of jasmonates in stress responses and development. I will

exclude roles of JA in the local and systemic wound response, of JA in mycor-

rhization, senescence, as well as cross-talk in JA, ET, salicylate, and ABA signaling.

Plant Stress Biology. Edited by H. HirtCopyright r 2009 WILEY-VCH Verlag GmbH & Co. KGaA, WeinheimISBN: 978-3-527-32290-9

| 91

These aspects have been reviewed in 2008 [9–12] and will also be covered by a

special issue of Phytochemistry appearing at the end of 2009.

5.2

JA Biosynthesis

JA and its derivatives are cyclopentanone compounds and are structurally similar to

prostaglandins – their counterparts in animals. Elucidated by Vick and Zimmer-

mann [13], biosynthesis of JA takes place by reactions similar to prostaglandin

biosynthesis. All of the enzymes of JA biosynthesis have now been cloned from

several plant species, leading to molecular and genetic tools for analyzing the mode

of action of jasmonates. The initial reaction is a release of a-linolenic acid (a-LeA),the substrate for JA formation, from galactolipids of chloroplast membranes.

Although phospholipase A2 (PLA2) was thought to function in JA biosynthesis [14],

today there is strong evidence that PLA1 and a galactolipase are active in JA bio-

synthesis. First, the Arabidopsis mutant dad1 (defective in anther dehiscence1)wasshown to be affected in a PLA1 accompanied by reduced JA levels in flowers,

diminished filament elongation, and, consequently, male sterility [15]. However,

the corresponding lipase in the leaves was still missing. Recently, a homolog of

DAD1, DGL (DONGLE; galactolipase), was characterized as a galactolipase with

weak PLA1 activity. DGL releases a-LeA from galactolipids of chloroplast mem-

branes, thereby providing the substrate for the basal level of JA in vegetative growth

and for the JA burst in early phases upon wounding [16]. a-LeA is the substrate of

the lipoxygenases 9-LOXs and 13-LOXs, which insert molecular oxygen at C-9 and

C-13, respectively, leading to hydroperoxy derivatives, which are further converted

in at least seven different branches of the LOX pathway [17]. JA originates from

(13S)-hydroperoxyoctadecatrienoic acid, which is converted by a 13-allene oxide

synthase (13-AOS) to an unstable allene oxide (Figure 5.1). Nonenzymatic cleavage

leads to a- and g-ketols, whereas an allene oxide cyclase (AOC) catalyzes the for-

mation of the cyclopentenone structure in OPDA. An interesting exception is the

tomato 9-AOS which acts in vitro as a multifunctional protein catalyzing with the

linoleic acid (9S)-hydroperoxide as substrate the formation of the corresponding

allene oxide, but also hydrolysis and cyclization of the allene oxide [18]. All of the

enzymes of OPDA formation (DGL, 13-LOX, 13-AOS, AOC) are located within the

chloroplast. Most of them carry an active target sequence, and chloroplast location

was proven by immunocytochemical analysis as well as import studies as for AOS

and AOC [19–24]. Conversion of OPDA into JA takes place in peroxisomes, which

requires transport of OPDA. So far an OPDA transporter is unknown, but the

partial JA deficiency of the CTS (COMATOSE) mutant upon wounding suggests

that CTS is involved [25]. CTS is an ATP-binding cassette (ABC) transporter also

known as PXA1/PED3 [26]. Within peroxisomes, OPDA is specifically reduced to

the corresponding cyclopentanone OPC-8 by the OPDA reductase OPR3 [27–29],

whereas OPR1 seems to reduce the nonenzymatically formed phytoprostanes [30].

Hypothesized for a long time, participation of the peroxisomal fatty acid b-oxidation

92 | 5 Jasmonates in Stress, Growth, and Development

Figure 5.1 Biosynthesis of JA in the chloroplast and

peroxisome. Reactions are described for conversion of a-LeA(18 : 3) via the intermediate OPDA. In a parallel pathway

leading to dnOPDA a 16 : 3 polyunsaturated fatty acid is the

substrate. Enzymes/proteins: At5g63380 and At1g20510, 4-CL-

like acyl-CoA synthetases; TE, thiolase; see text for other

abbreviations.

5.2 JA Biosynthesis | 93

in JA biosynthesis could be demonstrated recently. Acyl-CoA oxidase (ACX),

multifunctional protein (MFP), and 3-ketoacyl-CoA thiolase (KAT) were shown to

be involved in wound-induced JA formation by mutant analysis and transgenic

approaches [31–34]. Additional evidence was given by JA deficiency upon wound-

ing in pex6, an Arabidopsis mutant affected in an essential protein of peroxisome

biogenesis [34]. Although functional peroxisomes are essential for wound-induced

JA formation, the proliferation of peroxisomes is uncoupled from JA formation

[35]. The b-oxidative shortening of the carboxylic acid side-chain of OPDA needs

two additional reactions: (i) activation of the corresponding precursor to the CoA

ester and (ii) release of JA from its activated form jasmonoyl-CoA by a thioesterase.

An OPC-8 CoA ligase (OPCL1) contributes at least partially to wound-induced JA

formation [36]. Other activating enzymes were found among a clade of the

superfamily of adenylate-forming enzymes with similarity to 4-coumarate: CoA

ligases (4-CLs) [37, 38]. These 4-CL-like enzymes can activate OPDA [37], OPC-8,

and OPC-6 [38] (Figure 5.1).

The regulation of JA biosynthesis seems to be defined by at least five different

aspects: (i) substrate availability, since only induced substrate generation (e.g., by

wounding) leads to JA formation in AOS- or AOC-overexpressing lines [39, 40];

(ii) feed-forward regulation, since all genes encoding enzymes in JA biosynthesis

are JA-inducible [8]; (iii) specific location of the enzymes in distinct cell types or

even subcompartments of the chloroplast (e.g., of AOC in vascular bundles of

tomato, which differs from AOS and LOX) [41, 42]; (iv) different size of gene

families; and (v) activity control by protein–protein interactions in subcompart-

ments. The latter two aspects are less clear. The number of gene family members

for JA biosynthesis genes is strikingly different. LOX family members are first

distinguished by their specificity for oxygen insertion at carbon C-9 or C-13, thus

leading to many different oxylipins. Furthermore, additional specificity might be

given in the case of 13-LOXs by different location within the chloroplast sub-

compartments, thereby attributing to metabolic flux through the alternative

branches of the LOX pathway (e.g., the AOS branch and the hydroperoxide lyase

branch) [43]. Furthermore, interaction between AOS and AOCs is discussed based

on import studies for members of the A. thaliana AOC gene family [24] and a

proteome analysis of the inner envelope [44, 45].

Among the plant species, the number of gene family members of the AOSbranch exhibits interesting differences. In A. thaliana, there are one AOS and four

AOC genes, whereas in tomato, three genes encode AOSs, while AOC is encoded

by a single copy gene [22, 40, 46–48]. Consequently, in A. thaliana, JA biosynthesis

might be regulated downstream of the AOS spatially and temporally by individual

AOC isoforms. Initially, AOC was purified to homogeneity as a dimer [49]. The

crystal structure of the AOC2 of A. thaliana suggests that this protein occurs as a

trimer and is a member of the lipocalin family known to function in the transport

of small, hydrophobic molecules [50]. Therefore, hetero-homodimerization may

occur as an additional regulatory principle as shown for the nine isoforms of

1-amino-cyclopropane-1-carboxylic acid (ACC) synthase [51]. In summary, the four

isoforms of AOCs of A. thaliana represent a regulatory potential for the

94 | 5 Jasmonates in Stress, Growth, and Development

fine-tuning of JA formation. This is supported by promoter activities of AOC1–AOC4 recorded with promoter GUS (b-GLUCURONIDASE) lines during devel-

opment and in response to various stimuli [6], and by expression data in the public

databases. In contrast to A. thaliana, in tomato specificity for JA generation might

be given by the one AOC downstream of AOSs (three genes) and upstream of

OPRs (three genes). This is reflected in tomato AOC promoter activities appearing

in response to developmental and environmental stimuli [52]. Furthermore, spe-

cificity for JA formation is strengthened by a cell-specific location of AOC in

parenchymal cells of minor veins of tomato and within vascular bundles of main

veins and even in sieve elements [41, 42], supporting the idea that JA is active in

systemic signaling [4, 53]. The full scenario of regulation of JA formation

and action depends on two additional aspects, the metabolism of JA and

COI1 (CORONATINE-INSENSITIVE PROTEIN1)/proteasome-mediated signal-

ing, both of them described in the following sections.

5.3

JA Metabolism

As well as a basal level, JA accumulates transiently within the first hour in

response to external stimuli such as wounding and is frequently used as a marker

of stress responses linked to JA-induced alteration of gene expression. The initial

product of JA biosynthesis is (þ )-7-iso-JA, which equilibrates to the more stable

(�)-JA. However, numerous metabolites have been known for a long time and

were neglected in respect of JA responses due to their putative minor accumu-

lation. More recently, these metabolites have attracted great attention by hints for

specific functions as well as much more abundant occurrence than previously

detected. The following metabolites have been found so far (Figure 5.2): JAME,

the methyl ester of JA formed by a JA methyltransferase (JMT) [54], the JA amino

acid conjugates such as JA-Ile formed by JA : amino acid synthetase (JAR1) which

adenylates JA followed by exchange of the AMP moiety by an amino acid [55, 56],

11-hydroxy-JA formed possibly nonenzymatically and 12-hydroxy-JA (12-OH-JA)

formed by a so far unknown hydroxylase; 12-O-glucosyl-JA (12-O-Glc-JA) formed

by a so far unknown glucosyl transferase; sulfated 12-OH-JA (12-HSO4-JA)

formed in A. thaliana by the 12-OH-JA sulfotransferase AtST2a [57] and in tomato

by a SlST2a (Neumerkel and Wasternack, unpublished); several jasmonoyl-1-b-glucosyl esters [58], 12-OH-JA-Ile conjugate, possibly formed by JAR1 [59, 60], 12-

carboxyjasmonoyl-L-isoleucine [60], cis-jasmone formed by an unknown dec-

arboxylase [61] or possibly formed in a parallel pathway via iso-OPDA [62]; and

finally, the conjugate of JA with ACC [56]. Presumably, we can expect further JA-

derived compounds from various plant species (e.g., a 5u-(hydroxysulfonyloxy)-JAhas been recently isolated from a mangrove [63]).

The question on separate or overlapping signaling properties of JA and its

metabolites is of special interest. Transgenic approaches revealed that JAME is

only active upon its cleavage to JA [64]. In contrast, JA and JA-Ile showed

5.3 JA Metabolism | 95

independent gene expression responses [65]. For some of these metabolites, spe-

cific functions were identified. A prominent example is 12-OH-JA, also called

tuberonic acid due to its tuber-inducing properties in potato [66, 67]. Among other

compounds, a specific enantiomer of 12-O-Glc-JA is active as a leaf-closing factor

in Albizzia species [68]. These compounds bind in specific motor cells responsible

for nyctinastic movements [69], which require aquaporins [70]. It will be inter-

esting to see whether the enhanced JA levels observed in mechano-stimulated

Medicago truncatula plants [71] are accompanied by altered amount of 12-O-Glc-JA.

The volatile cis-jasmone is active in plant defense reactions [72]. A recent tran-

scriptome analysis revealed a specific set of genes induced by cis-jasmone, thereby

attributing it to specific behavioral responses of specialist and generalist insects

[73]. Signaling properties independent from JA were repeatedly described for

OPDA. Initially, tendril coiling of Bryonia was explained in terms of increased

OPDA levels [74]. Meanwhile several microarray analyses showed different sets of

genes expressed in response to OPDA or JA [30, 75, 76]. A clear answer on separate

signaling properties of OPDA and JA was already shown by plant defense reac-

tions in the JA-deficient mutant opr3 [77]. Most of these data led to the concept of

biological activity of compounds carrying a reactive a,b-unsaturated carbonyl

structure – the reactive electrophilic species. Among them there are OPDA and

phytoprostanes, but not JA [30, 78].

Figure 5.2 Metabolism of JA. Reduction of the keto group

within the cyclopentanone ring leads to cucurbic acid. The

pentenyl side-chain can be hydroxylated to 11-OH-JA and 12-

OH-JA, which is further converted to its sulfated or O-

glucosylated derivative. Also, isoleucine conjugates of 12-OH-

JA and a 12-carboxy-JA were found. The carboxylic acid side-

chain can be conjugated to the ET precursor ACC or to amino

acids such as Ile by the JA amino acid conjugate synthase

(Arabidopsis: JAR1; tobacco: JAR4), can be methylated by a

JMT, decarboxylated to cis-jasmone, or glucosylated to

jasmonoyl glucose ester. Enzymes cloned so far are framed.

96 | 5 Jasmonates in Stress, Growth, and Development

Until now it has been an open question how JA signaling can be switched off.

Recent data revealed that JA-induced inhibition of seed germination and root

growth are not caused by 12-OH-JA or 12-HSO4-JA [79]. Furthermore, both

compounds are unable to switch on expression of JA biosynthesis genes or wound-

inducible genes. This suggests that, as known for other plant hormones, hydro-

xylation of JA and subsequent sulfation inactivates JA [79]. In this respect, it is of

interest that both compounds and 12-O-Glc-JA occur abundantly in various organs

and tissues of different plant species at up to three orders of magnitude higher

levels than JA [79]. Finally, upon wounding of tomato leaves, 12-OH-JA, 12-HSO4-

JA, and 12-O-Glc-JA accumulate after JA to much higher levels than JA [79]. A

JA-dependent formation of 12-OH-JA was evidenced by mutants and transgenic

lines affected in JA biosynthesis [79]. A similar situation in respect of 12-OH-JA

accumulation was recently detected for A. thaliana. Here, a rapid burst in

JA accumulation upon wounding occurs, and is followed by accumulation of 12-

OH-JA, 12-OH-JA-Ile, and 12-HOOC-JA-Ile [60].

Obviously, hydroxylation inactivates JA, thereby counteracting the worse reg-

ulation of JA biosynthesis given by the positive feed-forward loop and substrate

generation upon wounding by ‘‘removal’’ of excess of the signaling compound JA.

5.4

Bound OPDA – Arabidopsides

The oxylipins derived from LOX activities occur either as nonesterified fatty acid

derivatives or are esterified to chloroplast membrane constituents [22]. In the

case of OPDA, the first substance was found in galactolipids (monogalacto dia-

cylglycerol (MGDG)) in the sn-1 position in untreated A. thaliana leaves [80].

These compounds were called arabidopsides according to their nearly exclusive

occurrence in Arabidopsis species [81]. Meanwhile, numerous types were found

(Table 5.1). They are derivatives of MGDG and digalacto diacylglycerol (DGDG),

respectively, and contain up to three OPDA and/or dinor (dn) OPDA residues.

Up to 17 species of oxylipin-containing phosphatidyl-glycerols, MGDGs, and

DGDGs were identified, including complex lipids with 18 : 3, 18-carbon ketol

acids and 16-carbon ketol acids beside the OPDA or dnOPDA moiety [82–84].

Presumably, some of the arabidopsides occur in thylakoid membranes as shown

by common localization with the photosystem I/II supercomplex, light-harvest-

ing complex II, and photosystem I [81]. Upon wounding, the amount of arabi-

dopsides (e.g., A, B, E, and G; Table 5.1) increase dramatically up to 1000-fold.

Furthermore, recognition of the phytopathogenic bacterial avirulence peptides

AvrRpm1 and AvrRPt2 led to a dramatic increase in arabidopside E up to 7–8%

of total lipid content [83], and arabidopside E inhibits growth of a bacterial

pathogen in vitro. Later, arabidopside G was identified and found to accumulate

also in response to the two bacterial effectors mentioned above as well as upon

wounding [84]. The formation of arabidopsides E and G was dependent on an

interaction of RPS2 (RESISTANCE TO PSEUDOMONAS SYRINGAE2) and

5.4 Bound OPDA – Arabidopsides | 97

NDR1 (NON-RACE-SPECIFIC DISEASE RESISTANCE1). Disease resistance and

salicylate (SA) signalingmutants such as rps2, ndr1, pad4sag101 (phytoalexin-deficient4and senescence-associated gene101) double mutant, sid2 (salicylic acid induction-defi-cient2), and npr1 (nonexpresser of pathogenesis-related (PR) genes1) were unaffected in

accumulation of these two arabidopsides. As expected by the wound-inducible accu-

mulation, both arabidopsides did not accumulate in the coi1 and jar1 mutants

(Table 5.2). Summarizing, these and additional data suggest that the pathogen- and

wound-induced accumulation of arabidopsides E and G is triggered by two signaling

pathways that converge in jasmonate signaling downstream of NDR1 and SA [84]. It

seems to be another example of cross-talk between SA- and JA-dependent signaling,

which can be antagonistic and synergistic [85]. The arabidopsides E and G may have

dual functions: (i) antipathogenic activity, and (ii) a role as storage compounds from

which OPDA and dnOPDA, respectively, can be released [80, 86]. In respect of the

different accumulation of the various arabidopsides upon various stimuli, we have to

consider more putative scenarios for the function of arabidopsides: (iii) JA-mediated

amplification in arabidopside formation and compensation of rapid flux in OPDA

synthesis by its esterification, and (iv) storage of newly formed OPDA and/or possible

exchange of the oxylipin residues between various arabidopsides. Whereas enzymes

of JA biosynthesis, such as LOX, AOS, and AOC, are inactive in vitro with their

esterified substrates [80], an adduct between LTP1b (LIPID TRANSFER PROTEIN1b)

and a toxic allene oxide 9-hydroxy-10-oxo-12(Z )-octadecanoic acid was found in barley

seeds [116]. It was generated by a 9-LOX and an AOS. Lipid transfer proteins are

ubiquitous suggested to be involved in diverse functions of plant development and

stress responses. However, their precise role is still unknown. Such adduct formation

between toxic oxylipins and lipid transfer proteins combined with the activity of

enzymes of JA biosynthesis is an interesting new facet of the functions of these

enzymes.

5.5

Mutants of JA Biosynthesis and Signaling

Since about 1995, several mutant screens have been initiated to pick up mutants

affected in JA biosynthesis and JA signaling (Table 5.2). Most of the mutants in JA

biosynthesis, at least in A. thaliana, are male-sterile and/or exhibit JA deficiency. As

Table 5.1 Arabidopsides and their constituents.

Arabidopside

A sn-1-OPDA, sn-2-dnOPDA-MGDG

B sn-1-OPDA, sn-2-OPDA-MGDG

C sn-2-dnOPDA-DGDGD sn-1-OPDA, sn-2-OPDA-DGDG

E sn-1-OPDA, sn-2-dnOPDA, Gal C-6-OPDA-MGDG

F sn-2-dnOPDA-MGDG (Ipomea)

G sn-1-OPDA, sn-2-OPDA, Gal-C-6-MGDG

98 | 5 Jasmonates in Stress, Growth, and Development

Table 5.2 Mutants and genes functioning in JA biosynthesis

and JA signaling in Arabidopsis and tomato.

Mutants Gene product Phenotype Reference(s)

JA biosynthesis

dgl galactolipase A1 Reduced JA level in leaves [16]

dad1 phospholipase A1 reduced filament elongation, male-

sterile, delayed anther dehiscence,

JA-deficient in flowers

[15]

fad3-2fad7-2fad8 fatty acid

desaturases

male-sterile, delayed anther

development, altered a-LeA level

[87]

spr2a o-3 fatty acid

desaturase

deficient in a-LeA and JA levels, no

wound response, suppressed

prosystemin expression

[88]

aos AOS JA-deficient, decreased resistance to

pathogens

[89]

dde2-2 AOS male-sterile, delayed anther

development

[90]

opr3 OPR3 JA-deficient, decreased resistance to

pathogens, reduced filament

elongation, male-sterile

[28]

dde1 OPR3 JA-deficient, reduced filament

elongation, delayed dehiscence

[91]

acx1a acyl-CoA oxidase JA-deficient, reduced wound

response

[92]

aim1 multifunctional

protein 1

abnormal flower meristem, reduced

fertility

[93]

comatose CTS/PXA1 ABC

transporter

Reduced JA content [94]

Constitutive JA

response

cev1 cellulose

synthase CES3

constitutive expression of vegetative

storage proteins

[95, 96]

cet1-9 ? constitutive expression of thionins,

increased JA levels

[97]

cex1 ? constitutive root growth inhibition,

constitutive expression of JA-

responsive genes

[98]

cas1 ? constitutive expression of AOS [99]

joe1 ? increased expression of LOX2,increased accumulation of

anthocyans

[100]

hy1-101 heme oxygenase

HY1

increased JA level, stunted growth,

phytochrome chromophore

deficiency

[101]

joe2 ? reduced inhibition of root growth,

increased expression of LOX2[100]

Others

ore9, max2 F-box protein [102, 103]

(continued )

5.5 Mutants of JA Biosynthesis and Signaling | 99

discussed below, male sterility is preferentially caused by the role of JA for proper

filament elongation and/or an essential role of a-LeA content of the tapetum for

proper anther development and pollen dehiscence. Another common phenotype of

JA deficiency is a decreased resistance to pathogens and diminished wound

response. In the case of signaling mutants, altered sensitivity to JA (e.g., in root

delayed leaf senescence, more

axillary branches

cos1 lumazine

synthase

suppressors of JA-dependent

defects in coi1 (root growth,

senescence, defense)

[104]

Reduced

sensitivity to JA

coi1 F-box protein

COI1

reduced root growth inhibition,

male-sterile, reduced filament

elongation, enhanced sensitivity to

necrotrophic pathogens

[105, 106]

coi1-16 F-box COI1 þPEN2, a glycoside

hydrolase

COI1 phenotype þ loss of

penetration resistance of pathogens

[107, 108]

jai1a) tomato homolog

of COI1

female-sterile, altered trichome

development, increased sensitivity

to pathogens, decreased wound

response

[109]

jar1/jin4/jai2 JA amino acid

conjugate

synthase

reduced root growth inhibition by

JA, increased sensitivity to

necrotrophic pathogens

[55, 56,

110]

jin1/jai1 AtMYC2 (basic

helix–loop–helix

zip transcription

factor)

reduced root growth inhibition [111]

jai3 reduced root growth inhibition in

ein3 background

[111]

jue1-3 ? reduced expression of LOX2 [100]

oji ? enhanced sensitivity to ozone,

reduced root growth inhibition

[112]

mpk4 AtMPK4 dwarf phenotype, altered expression

of JA- and SA-response genes,

reduced sensitivity to JA, ET and

ABA, impaired in ozone signaling

[113]

rcd1 radical-induced

cell death 1

[114]

axr1 RUB (related to

ubiquitin)-

activating

enzyme

reduced root growth inhibition by

JA

[115]

jai4/sgt1b AtSGT1b reduced root growth inhibition in

the ein3 background

[111]

aTomato mutants.

Modified after [1] and [7].

100 | 5 Jasmonates in Stress, Growth, and Development

growth inhibition) and screens with JA-responsive promoter-reporter lines (e.g.,

promoters of LOX2, VSP (VEGETATIVE STORAGE PROTEIN), or Thi2.1 (THIO-NIN2.1)) have been used. These screens led to the isolation of mutants with a

constitutive JA response or with reduced sensitivity to JA. Cloning of the affected

genes led to identification of exciting new JA signaling components. One of the first

identified mutants was coi1 (coronatine-insensitive1), which is affected in the F-box

protein COI1, the key player in JA signaling [105] (see Section 5.6). Another example

is the jar1 (jasmonate-resistant1)mutant, whichwas first identified in 1992 by the root

growth inhibition assay [110]. Identification of the affected gene took more than a

decade due to the minor sequence homology to known A. thaliana genes. The cor-

responding gene is amember of a superfamily that codes for enzymes adenylating a

carboxylic acid with subsequent transfer to a second substrate. In the case of JAR1,

the substrates are JA and amino acids such as Ile leading to the JA-Ile conjugate [55,

56]. The fact that lack of JA-Ile, but not JA, affects JA signaling shed exciting new

light on the mechanism of JA signaling. Now, we can understand these aspects at

least partially by the COI1–jasmonate ZIM domain (JAZ)–JA-Ile interaction (see

Section 5.6). Finally, identification of cev1 (constitutive expression of vsp1) as a mutant

affected in the subunit 3 of the cellulose synthase was important, since a link

between cellulose synthesis/cell elongation and JA signaling was found, including

elevated levels of jasmonates [95, 96].

5.6

COI1–JAZ–JA-Ile-Mediated JA Signaling

In 1998, COI1 was identified as an F-box protein [105]. The coi1 mutant exhibits

defects in numerous JA-dependent processes such as biosynthesis of secondary

metabolites, pathogen and insect resistance, fertility, and wound responses. Since

2000, gene expression data have accumulated showinghowmanygenes are expressed

in a COI1-dependent manner [117–120]. Another key player in JA signaling was

identified by analysis of the mutant jin1( jasmonate-insensitive1)/myc2. JIN1/MYC2(henceforth referred to asMYC2) encodes a basic helix–loop–helix transcription factor[111], which is involved in positive and negative regulation of JA-dependent tran-

scriptional activation [121]. Since the identification of COI1, JA-induced gene

expression was explained in terms of a repressormodel, where a negative regulator is

degraded via the SCFCOI1 complex (SKP1 (S-PHASE KINASE-ASSOCIATED PRO-

TEIN1), Cullin, F-box protein E3, ubiquitin ligase) and the 26S proteasome. Among

the components of the SCFCOI1 complex, COI1 is the specificity-determining subunit

that selectively recruits target proteins which were unknown until recently.

Three independent approaches led to the identification of a gene family of

previously unknown function, coding for ZIM domain proteins [122]:

1. A subgroup of 12 members, the JAZ proteins, was found by rapid expression of

their corresponding genes in flower filaments upon JA treatment of the opr3mutant [123]. In addition to the ZIM domain, JAZ proteins carry the highly

conserved Jas motif near the C-terminus.

5.6 COI1–JAZ–JA-Ile-Mediated JA Signaling | 101

2. The dominant jai3 (ja-insensitive3) mutant was characterized as a splicing

defect in JAZ3 leading to lack of the Jas motif in JAZ3 [124]. Consequently,

interaction of JAZ3 with MYC2, a central regulator in JA-induced gene

expression, is lost [124].

3. Finally, overexpression of an isoform of JAZ10 that carries an incomplete Jas

motif led to diminished repression of JA-regulated growth retardation [125].

All three approaches together with the previously identified JA-Ile-forming

activity of JAR1 suggested a model of JA signaling via the SCF complex, where

COI1, JAZ proteins, MYC2, and JA-Ile are key players [10, 12] (Figure 5.3). Under

uninduced conditions JA-responsive genes are repressed by the negative reg-

ulators JAZs, which inhibit at least MYC2. Upon an environmental stimulus such

as wounding, an endogenous rise of JA occurs rapidly as discussed above. It is

conjugated at least partially to JA-Ile by JAR1 [56]. Most interestingly, JA-Ile but

not or much less other JA amino acid conjugates increases in vitro interaction of

Figure 5.3 The JAZ–COI1-directed proteasome. JA-induced gene

expression is switched on by the transcription factor JIN1/

MYC2. However, without an external signal JIN1/MYC2 is

repressed by JAZ protein(s). In the presence of JA-Ile generated

by JAR1 upon endogenous rise of JA in response to

environmental factors, JAZ protein(s) can interact with the F-box

protein COI1. COI1 is a member of the SCF complex consisting

of the SKP1/ASK proteins, a Cullin, and the F-box protein. Upon

JA-Ile-mediated interaction of JAZ and COI1, JAZ is ubiquitinated

and degraded by the 26S proteasome, thereby liberating JIN1/

MYC2 from its repressor and allowing JA-induced gene

expression (see text for details) (designed by B. Hause).

102 | 5 Jasmonates in Stress, Growth, and Development

COI1 and JAZ1 within the SCFCOI1 complex [123]. Recently, (þ )-7-iso-JA-L-lle wasshown to be the most bioactive jasmonate compound in COI1-JAZ-interactions

suggesting that the active ligand of the JA receptor is formed by epimerization in a

narrow time window [158]. Subsequently, the repression of MYC2 by JAZ proteins

is lost, since JAZ proteins are directed to degradation via the 26S proteasome.

Many details are in agreement with this repressor model in JA signaling:

1. Overexpression of JAZ genes did not affect JA signaling.

2. JAZ1, JAZ3, JAZ10, and MYC2 were found to be located in the nucleus [123–

125].

3. JAZ1 and JAZ3 interact with COI1, if the Jas motif is present and if JA-Ile is

available.

4. JA signaling is lost in the mutants myc2, coi1, and jar1, and the jaz mutants

lacking the Jas motif.

5. JAZ proteins have overlapping functions since jaz knockout mutants do not

show any JA phenotype such as growth retardation.

6. JAZs, MYC2, and some JA biosynthesis genes are primary response genes,

which are rapidly upregulated if the COI1-dependent turnover of a labile

repressor (JAZ) is blocked by cycloheximide [126].

The COI1–JAZ–JA-Ile interaction and JAR1 as well as MYC2 activity seems to be

conserved among species (e.g., all components and analogous interactions have

been found in tomato) [123, 126, 127]. JAZ genes are rapidly induced by JA, several

of them in a MYC2-dependent manner. Consequently, JAZ degradation will

facilitate expression of themselves, representing a classical negative loop [12]. On

the other hand, MYC2 expression is negatively regulated by its own expression

[121]. Obviously, the regulatory interplay among the key components in JA sig-

naling is sustained by positive and negative regulation, allowing a proper time

window and strength of interaction. Moreover, the complete scenario described in

Figure 5.3 seems to be not essential for wound-induced expression of JAZ genes,

of several JA biosynthesis genes, and of wound-responsive genes such as PDF1.2(a plant defensin) or VSP2 [126, 128]. Although they are expressed COI1-depen-

dently, their expression does not require JAR1.

Different specificity of JAZ proteins with respect to the activation by the various

JA compounds may occur. However, most of them interact in vitro with COI1

preferentially in the presence of JA-Ile [12]. So far, there is no clear mechanistic

explanation for JA- and OPDA-specific gene expression, which has been repeatedly

observed [30, 75–77].

Meanwhile, mechanistic details of interaction of JA-Ile with the tomato

COI1–JAZ complex could be found [12]. Binding and competition assays with

coronatine and the COI1–JAZ3 complex showed 100-fold higher activity of cor-

onatine compared to JA-Ile [12]. Coronatine, a virulence factor of P. syringae, isregarded as a molecular mimic of JA-Ile [10] and was used in the initial screens on

JA-insensitive mutants such as coi1. The much stronger binding of coronatine than

of JA-Ile indicates that the stabilized ring structure in coronatine is important. The

stronger binding of coronatine highlights another important aspect of interaction of

5.6 COI1–JAZ–JA-Ile-Mediated JA Signaling | 103

the coronatine-producingP. syringaewith the host. By exploiting the host’s hormone

signaling pathways (e.g., JA), the pathogen promotes infection [12]. In tomato,

the homolog of COI1 is JAI1 (Table 5.2). The jai1-3 tomato mutant carries a point

mutation in Leu418 of the leucine-rich repeat. Interaction of coronatine with the

COI1–JAZ3 complex was strongly reduced in leaf extracts of jai1-3 plants, sug-

gesting that the complex is an active JA receptor [12]. These data fit the initial

suggestion that COI1 might be the JA receptor [129]. This idea came up upon

identification of TIR1 (TRANSPORT INHIBITOR RESPONSE1) as the auxin

receptor and its homology to COI1 [130, 131]. Surprisingly, themutated Leu residue

in jai1-3 is in a similar position as Ile406 in TIR1, where the auxin/indole acetic acid

substrates are recognized in the auxin-binding pocket [134]. The critical role of COI1

for a JA receptor function is strengthened by the fact that its complex with JAZ3

requires the C-terminal region, where the highly conserved Jas motif is located [12].

In amost recent work on this Jasmotif, two positively charged amino acids of the Jas

domain in JAZ1 were identified to be essential for JA-Ile-(coronatine)-dependent

JAZ–COI1 interaction, but not for JAZ–MYC2 interaction [133]. This was supported

by a very strong JA-insensitive phenotype of mutants lacking these amino acids.

The ongoing work on the JA receptor will cover its crystallization and further

structure–activity tests. However, a striking similarity is already obvious in the

type and sequences of components of the auxin receptor TIR1 and the JA receptor

COI1. These aspects of the conserved mechanism of hormone sensing are dis-

cussed in the most recent review on COI1–JA-Ile–JAZ interaction [12].

5.7

Transcription Factors Involved in JA Signaling

MYC2 is a central regulator in positive and negative regulation in JA signaling as

shown by expression analyses [9, 111, 121]. Its important role is also indicated by

physical interaction of MYC2 with JAZ proteins (Figure 5.3) [123, 124]. These data

place MYC2 downstream of COI1 (Figure 5.4). Among genes expressed upon her-

bivory or pathogen attack via COI1 and MYC2 are those encoding enzymes in jas-

monate and flavonoid biosynthesis andmetabolism, encoding proteinase inhibitors

(PINs) and other wound-/herbivore-induced proteins such as VSP, LOX, Thi2.1, or

proteins active in oxidative stress tolerance [119, 121]. Genes repressed by MYC are

active in pathogen defense such as PR1, PDF1.2, b-CHI (BASIC CHITINASE), orHEL (HEVEIN), and in tryptophan biosynthesis and tryptophan-dependent gluco-

sinolate metabolism [9, 121]. Furthermore, MYC2 is known to mediate cross-talk in

both JA/ABA as well as JA/SA signaling [9, 111]; for example, the ABA-dependent

drought response is downregulated by MYC2 [134] and JA biosynthesis is upregu-

lated by ABA [135]. An interesting facet of MYC2 activity is its position downstream

of the mitogen-activated protein kinase (MAPK) pathway regulated by the MAPK

kinaseMKK3 and theMAPKMPK6 [136] being active in parallel to anMKK3/MPK6-

independent branch (Figure 5.4). The diverse functions of MYC2 suggest that

additional transcription factors are required to define the positive and negative

104 | 5 Jasmonates in Stress, Growth, and Development

regulation by MYC2. Indeed, transcription factors such as ERF2 (ETHYLENE-

RESPONSIVE FACTOR2), ERF6, ERF11, WRKY26, WRKY33, MYB51, and

MYB109 seem to be involved in MYC2-regulated gene expression [121]. Important

counterparts of MYC2 are in the ERF family – a subgroup of the large AP2 (APE-

TALA2)/ERF superfamily [137]. ERF1 acts as a COI1-dependent transcription fac-

tor, which upregulates antagonistically to MYC2 defense genes such as PDF1.2 or

b-CHI, thus being an integrator of JA and ET signaling [111]. Other members of the

ERF family are the ORA (octadecanoid-responsive Arabidopsis AP2/ERF) tran-

scription factors. One of them, ORA59, was recently identified as being partially

redundant to ERF1 [139]. ERF1 andORA59 are expressed in response to JA and ET,

act downstream of COI1, and lead to expression of defense genes such as PDF1.2;however, ORA59, even partially redundant to ERF1, is essential [138]. Other

members of theORA family areORA33,ORA47, andORA37 [139]. ORA47 has been

characterized as a key transcription factor in the positive-feedback loop of JA bio-

synthesis with LOX2, AOC2, and OPR3 as primary targets. ORA33 positively reg-

ulates tryptophan biosynthesis and secondary metabolism, whereas ORA37 acts

antagonistically to ORA59 and ERF1, thus repressing PDF1.2 expression, but

inducing VSP, LOX, and Thi2.1 expression [141]. ERF1, ORA59, ORA33, ORA37,

Figure 5.4 Different regulation of JA-dependent processes by

JIN1/MYC2. Positive regulation is indicated by arrows,

negative regulation is indicated by blunt arrows. TFs,

transcription factors. Adapted from [9].

5.7 Transcription Factors Involved in JA Signaling | 105

andORA47 areCOI1-dependently expressed, but an interactionwith JAZproteins is

yet unknown.

Due to the diverse regulatory roles of MYC2 in transcriptional activation an

intriguing question is which signaling component functions downstream

of MYC2. Recently, members of the NAC (NAM/ATAF1,2/CUC2) protein family

of plant specific transcription factors were identified as targets of MYC2. AtNAP

was found to be involved in leaf senescence [140]. NAC019 and NAC055 function

COI1-dependently downstream of MYC2 as transcriptional activators of JA-

responsive genes [141]. NAC019 interacts with the CATGT and CACG motifs in

the promoter of the AtVSP1 gene. This scenario is consistent with the above-

mentioned regulation of transcription factors such as ERF2, ERF6, ERF11,

WRKY33, and MYB109 by MYC2. Interestingly, genes encoding these factors carry

enrichments of strong MYC2-binding sites such as CACNGT, a core motif, as well

as CACGTG and CACATG in their upstream region [121]. Although orchestrated

with respect to the regulatory output, the key players in JA signaling seem to

function in a hierarchical order: there are MYC2, other transcriptions factors such

as NAC019, NAC055, and ERF2, and any JA-responsive gene, each of them

functioning downstream of the former component. Another important class of

plant-specific transcription factors is the WRKY family characterized by the pre-

sence of a DNA-binding domain containing the conserved WRKYGQK sequence

and a zinc finger motif [142]. Several of the 74 WRKYs such as WRKY53,

WRKY33, WRKY62, and preferentially WRKY70 mediate the cross-talk between

SA and JA downstream of NPR1 and COI1. These aspects were recently reviewed

in detail [9, 11, 120, 121]. Apart from transcription factors, Ca2þ signaling was

found as a regulatory element. It will be interesting to see whether the altered

oxylipin formation in the flou2 mutant is caused by an affected putative Ca2þ

permeant nonselective cation channel [143, 144, 145].

5.8

Jasmonates and Oxylipins in Development

Mainly by identification of mutants in JA biosynthesis and JA signaling, the roles

of JA in various developmental processes became obvious (Table 5.2). Among

them there are root growth, seed germination, tuber formation, tendril coiling,

nyctinasty, trichome formation, senescence, and different aspects of flower

development [8].

Apart from the already mentioned tuber formation, tendril coiling, and nycti-

nasty (see Section 5.3), only few recent data on JA in root growth and flower

development will be discussed here.

Root growth inhibition by JA was one of the two first JA responses observed

[110, 146], and several screens to isolate mutants in JA biosynthesis and signaling

or cross-talk to other hormones were based on this assay [2]. There is, however, no

final mechanistic explanation for root growth inhibition by JA. Involvement of

components in JA signaling such as COI1, MYC2, JAI4/SGT1b, and AXR1

106 | 5 Jasmonates in Stress, Growth, and Development

(AUXIN-RESISTANT1) was suggested by mutant phenotypes and gene expression

data (e.g., mutants with constitutively elevated levels of JA such as cev1 (Table 5.2)

have reduced root length and a stunted growth phenotype as occurring upon JA

treatment). Many of the genes encoding enzymes in JA biosynthesis are expressed

in the elongation zone, which corresponds to upregulation of JA-responsive genes

in these tissues [147]. Root elongation is preferentially defined by auxin home-

ostasis [148]. However, there are several examples on antagonistic cross-talk in

auxin/JA signaling. Interestingly, increased AOC promoter activity, which corre-

lates with an increase in JA formation, was found in the elongation zone of roots of

10-day-old tomato seedlings [52]. This AOC promoter activity was inhibited by IAA

and inhibition was compromised by the antiauxin p-chlorophenoxyisobutyric acid.It is tempting to speculate on an antagonistic interaction of auxin and JA based on

gene expression data [120]. Furthermore, a cross-talk between auxin and JA sig-

nalling was explained mechanistically by auxin-dependent JAZ1 expression [159]

as well as by jasmonate–induced auxin biosynthesis via expression of ANTHRA-NILATE SYNTHASE a1 [160].

The most significant proof for a role of JA in flower development was given by

mutants affected in JA biosynthesis and signaling (Table 5.2). In the case of

Arabidopsis mutants, male sterility was caused among other aspects by insuffi-

cient filament elongation as shown for dad1 and opr3 [15, 28]. Reduced filament

length correlated with a decrease in JA levels at the corresponding flowering stage

(dad1). Interestingly, the arf6/arf8 (auxin response factor6/auxin response factor8)double mutant impaired in two auxin response factors showed reduced JA levels

in the mutant filaments [149], suggesting auxin-dependent JA formation in

flowers. A first explanation was given by identification of the JA-inducible tran-

scription factors MYB21 and MYB24 as key regulators of proper stamen devel-

opment [150]. This was strengthened by the observation that AGAMOUS controls

late stamen development via the expression of JA biosynthesis genes [151].

AGAMOUS is a homeotic C-class gene encoding a MADS-box transcription fac-

tor. Genetic and biochemical evidences were found that AGAMOUS directly

regulates DAD1 expression, thus affecting JA generation in stamens. This sce-

nario on JA action in stamen development is supported by a similar pattern of

promoter activities of AOC and that of JA-responsive genes such as Thi2.1 and

aquaporin AthH2 [6, 152, 153].

Another interesting aspect is the variable pattern of jasmonates in different

flower organs [41]. The total amount and ratio of jasmonates can vary remarkable,

which is called the ‘‘oxylipin signature.’’ Since the amount is elevated by con-

stitutive overexpression of tomato AOC, regulation of JA biosynthesis seems to

differ between flowers and leaves, where additional substrate generation is

necessary [154]. The role of JA in flowers is also indicated by the sequential action

of the following events, all of them proven experimentally: accumulation of glu-

cose in the nonphotosynthetic ovules which represents a sink-tissue - glucose-

induced AOC promoter activity; AOC expression and AOC protein accumulation

preferentially occurring in ovules - abundant accumulation of jasmonates in

ovules - expression of JA-inducible plant defense genes such as those for PIN2,

5.8 Jasmonates and Oxylipins in Development | 107

threonine deaminase, or leucine amino peptidase - increased defense status of

ovules as shown by lower infestation by insects [41, 52, 155–157].

A surprising result was the female sterility of the tomato mutant jai1, which is

affected in a gene homologous to COI1 of Arabidopsis [109], where the corre-

sponding Arabidopsismutant coi1 is male-sterile (Table 5.2). Both genes encode the

F-box protein COI1 essential for JA signaling (Figure 5.3). The fact that func-

tionally identical proteins lead to different signaling outputs in different genetic

backgrounds gives rise to interesting future questions for resolving signaling

pathways and their evolution.

5.9

Conclusions

The central role of jasmonates in plant stress responses and development has been

established in the last decade. Future work will give insights into the mechanism

of activity of signaling components by analysis of their crystal structure, by deeper

analysis of the regulatory network of jasmonate-induced gene expression,

including its cross-talk to other plant hormones. New aspects will be the simila-

rities and divergences in the jasmonate-dependent regulatory network in response

to different biotic stressors, but also natural variegation will come into the focus of

the jasmonate research. Finally, new techniques in the analyses of jasmonates will

help to find new active and inactive jasmonate compounds, thus helping us to

answer the question, ‘‘How is jasmonate signaling switched on and switched off?’’.

Acknowledgments

I apologize for references not cited due to space limitations. The research in the

author’s own laboratory was funded by the Deutsche Forschungsgemeinschaft

(German Research Foundation) within the SFB 363 project C5; the SFB 106

project C2; the SPP 1067, WA 875/3-1/2/3, WA 875/6-1; and the graduate program

(TP13) of the excellence initiative ‘‘Biosciences’’ of Sachsen-Anhalt. I thank

C. Dietel for typing the manuscript, C. Kaufmann for help in the design of the

figures, B. Hause, M. Quint, and I. Feussner for critical reading, and all members

of the laboratory for fruitful scientific activities.

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