biosynthesisandactionof jasmonates in plants · walls, and by peptide inducers such as systemin...

1040-2519/97/0601-0355$08.00

355

CREELMAN & MULL ETBIOSYNTHESISAND ACTION OF JASMONATESAnnu.Rev. Plant Physiol. Plant Mol. Biol. 1997. 48:355–81Copyright© 1997by AnnualReviewsInc. All rightsreserved

BIOSYNTHESISAND ACTION OFJASMONATESIN PLANTS

Robert A. Creelmanand John E. MulletDepartment of Biochemistry and Biophysics, CropBiotechnologyCenter, TexasA&MUniversity, CollegeStation, Texas77843

KEY WORDS: jasmonic acid, chemistry, gene expression, insectanddisease resistance

ABSTRACT

Jasmonicacid anditsderivativescanmodulateaspectsof fruit ripening,produc-tion of viablepollen, rootgrowth, tendril coil ing,and plant resistanceto insectsand pathogens. Jasmonate activates genes involved in pathogen and insectresistance,andgenesencodingvegetative storageproteins, but repressesgenesencoding proteins involved in photosynthesis. Jasmonic acid is derived fromlinolenic acid, and most of the enzymes in thebiosynthetic pathway have beenextensively characterized. Modulation of lipoxygenaseandallene oxide syn-thase gene expression in transgenic plants raises new questions about thecompartmentation of thebiosynthetic pathway andits regulation.Theactivationof jasmonic acid biosynthesisby cell wall elicitors, the peptidesystemin, andother compoundswil l berelatedto thefunctionof jasmonatesin plants.Jasmon-atemodulatesgeneexpression at thelevel of translation, RNA processing, andtranscription.Promoterelementsthat mediateresponsesto jasmonatehavebeenisolated. This review covers recent advances in our understanding of howjasmonate biosynthesis is regulated and relatesthis information to knowledgeof jasmonatemodulated geneexpression.

CONTENTSINTRODUCTION..................................................................................................................... 356CHEMISTRY AND QUANTITATION................................................................................... 356JA ACCUMULATI ON AND DISTRIBUTION ...................................................................... 358BIOSYNTHETIC PATHWAY AND REGULATION ............................................................ 360

Linolenic Acidand Lipases................................................................................................. 361Lipoxygenase(LOX)............................................................................................................ 363

AlleneOxide Synthaseand Other Stepsin JABiosynthesis................................................ 364JASMONATESIGNAL TRANSDUCTION .......................................................................... 365JA FUNCTION AND RESPONSIVEGENES........................................................................ 367

SeedGerminationand Growth............................................................................................ 367VegetativeSinksand StorageProteins................................................................................ 368Photosynthesis,Senescence, and Abiotic Stress.................................................................. 369Flowerand Fruit Development........................................................................................... 371Insectand Disease Resistance............................................................................................. 372JA’s Dual Role in Development and Defense..................................................................... 373

CONCLUDING REMARKS.................................................................................................... 375

INTRODUCTION

Jasmonicacid (JA), and its methyl ester(methyl jasmonate, MeJA) are li -nolenicacid(LA)-derivedcyclopentanone-basedcompoundsof wide distribu-tion in the plant kingdom. MeJA was first identified as a componentof theessentialoil of several plantspecies,while JA was firstobtainedfrom a fungalculturefiltrate. Early studiesshowedthatexogenousJA or MeJA canpromotesenescenceandactasagrowthregulator.SubsequentresearchrevealedthatJAspecificallyalters geneexpression and that wounding and elicitors could causeJA/MeJAaccumulationin plants.Theseresultsimplieda role forjasmonateinplantdefensethathasrecentlybeenconfirmed.Otherresearchdescribedrolesfor jasmonatesin vegetativedevelopment,fruit development, and pollen vi-ability. Thedual role of JA in plant developmentanddefenseis examinedinthis review.This reviewemphasizesnewinformation in this field sincethelastreview in this series(103). Other excellentreviewsare availablethat coverJA/MeJAwith respectto herbivory(7, 13),signaling(40,106),chemistryandbiochemistry (51, 56), geneexpression(89), andchromatography(117). Forthe purposesof this review, (3R, 7RS)-JA/MeJAwill be referredto collec-tively as jasmonates unlessit is necessary toidentify specificisomers.

CHEMISTRY AND QUANTITATION

The jasmonatemolecule(Figure1) containstwo chiral centerslocatedat C3andC7 generatingfour possiblestereoisomers,sinceeitherchiral centercanhaveanR or Sabsoluteconfiguration. Themirror imageisomers,(3R, 7S)and(3S,7R), havetheir sidechainsin a cis orientation. Theseisomersareknownas(+)− and(−)-7-iso-JAor (+)− and(−)-epi-JA.The enantiomers,(3R, 7R)-and (3S, 7S)-JA or (−)-JA and (+)-JA, have their side chainsin the transconfiguration.Becauseof increasedsterichindrance,thecis orientation is lessstableandwill epimerizeto the morestabletrans configuration.This occursvia a keto-enoltautomerization involving theC6 ketoneandtheC7 protonto

356 CREELMAN & MULLET

form thecorrespondingdiastereomers.During extractionor in thepresenceofacids or bases,(+)-7-iso-JA, thought to be the initial jasmonateformed inplants, is believed to epimerizeto anequilibriummixtureof approximately 9:1(−)-JA:(+)-7-iso-JA (80). The actual equilibrium concentrationin planta isunknown.Consequently, analysisof jasmonatesisolatedfrom plantsshouldindicatewhich isomersarebeinganalyzed.Commercially availablesyntheticMeJA usedin manyexperimentsis composedof a 9:1 ratio (±)-MeJA:(±)-7-iso-MeJA.The methyl estersmay be convertedto the free acidswith eitherbasic hydrolysis or incubation with commerciallyavailable esterases.

Figure 1 Chemicalstructuresof various isomersof jasmonic acid andcoronatine. The 3S, 7Sisomeris the final product of the jasmonic acidbiosynthetic pathwayandis easily convertedto itsdiastereomer3R,7Sisomerduringextraction.Thecorrespondingenantiomersarefoundin syntheticmaterial. Coronatineis a bacterialphytotoxin with biological activities similar to jasmonic acid.

BIOSYNTHESIS AND ACTION OFJASMONATES 357

A monoclonalantibodyfor theanalysisof (−)-JA (analyzedasthemethylester)hasbeendescribed(1). Assuming that(−)-MeJA hasa crossreactionof100%,(+)-7-iso-MeJAhada crossreactivity of 86%. Albrecht et al (1) sug-gestedthat, when using this monoclonal antibody, it is advisableto allowendogenousjasmonatesto reachtheir stableequilibrium beforequantitation.Furthermore,as is the casewith any antibody-basedtechnique,proceduresmustbe developedto estimatelossesduring extraction.In addition,antibodymethodsmustbevalidatedusinga physicalmethodsuchasGC-MSto checkfor possibleerrors due tointerferingcompoundspresent inextracts.

SyntheticJA or jasmonateanalogscontainingdeuteriumor 13C havebeenusedto quantify endogenousjasmonatesby GC-MS selectedion monitoring.The jasmonate diastereomerscan be resolvedby gaschromatographyusingcapil lary columns enabling their separate quantitation. Furthermore, massspectraof endogenouscompoundscan be to usedto unequivocallyidentifyjasmonatesbasedon comparisonwith publishedspectra.Mueller and Brod-schelm(80) derivatizedjasmonatesto thepentafluorobenzylestersfor quanti-tation by GC-MS-NICI and reporteda limit of detectionof ∼500 fg. Thepresenceof the fluorine atomsaccountsfor the increasedsensitivity of thismethod.Creelmanet al (29) used(13C,2H3)-MeJA, whereasGundlachet al(53) used9,10 dihydrojasmonicacid to estimateJA levels.However,useofcompoundsthatarestructurally similar to thecompoundbeingmeasuredmayunder-or overestimateendogenouslevelsunlessthe recoveryefficienciesareidentical.To circumventthis problem,Creelman& Mullet (28) synthesized(2-13C)-JA andusedit to measureJA in soybeantissue.Useof (2-13C)-JA incalculating endogenouslevels ofJA musttakeinto accountthem/e225(M+1)in isotopedilution calculationsbecauseof the natural abundanceof heavyisotopes.A significantimprovementwasthesynthesis of (1,2-13C)-JA with amolecularweight two massunitshigherthanendogenousJA (Z-P Zhang,ESMcCloud& IT Baldwin, personalcommunication).Thepositive andnegativeion electrospraymassspectraof severaljasmonateaminoacidconjugatesweredeterminedby combined HPLC-MS (102).

JAACCUMULATION AND DISTRIBUTION

Thelevel of JA in plantsvariesasa functionof tissueandcell type,develop-mentalstage,and in responseto severaldifferent environmental stimuli. JAlevelsarelow in soybean seedsbut increaseto 2µg/g fresh weightin develop-ing axeswithin 12 h of imbibition. In soybeanseedlings, levels of JA arehigher in the hypocotyl hook, a zoneof cell division, and young plumulescomparedto thezoneof cell elongation andmorematureregionsof thestem,


older leaves,and roots. High levels of JA are also found in flowers andpericarp tissuesof developingreproductivestructures (28,71).

In mature soybeanleaves, highlevelsof jasmonate responsive geneexpres-sion areobservedin paraveinalmesophyll cells andbundlesheathcells thatsurroundveinsandto a lesserextentin epidermalcells(50,61).Littl e expres-sion of jasmonateresponsivegenesis observedin palisadeparenchymacellsunlessleavesaretreatedwith jasmonate(61). This suggeststhatJA levelsarelower or compartmentalizeddifferently in palisadecellsor that thesecellsarelesssensitiveto JA. In illuminatedplants,JA will accumulatein chloroplastsbecauseit is a weakacid,assumingit becomesdistributedin cellularcompart-mentslike ABA (58). Becausepalisadecellsarefilled with chloroplasts,thismay lower the level of JA in thecytoplasmof thesecellsbelowthethresholdneeded toactivate gene expression.

The accumulation of JA in chloroplastsmay help explainwhy exogenousJA activatesgeneexpressionbut increasingendogenouslevelsof JA by over-expressionof alleneoxide synthasedoesnot (57). ExogenousJA will causetransientand large changesin the concentrationof JA in most plant cellsbeforereachinginternalequilibrium in tissues.In contrast,over-expressionofalleneoxide synthasein chloroplastsprovidescells with elevatedratesof JAsynthesisover the life of the plants.JA is synthesizedin theseplantsin cellscontainingchloroplasts whereit canbesequesteredasit is produced.This maykeep the levelof JA from risingin other regionsof thecell whereJA receptorsthatmodulategene expressionare presumablylocated.

Jasmonate levelsarerapidly andtransiently increasedby mechanicalper-turbationssuchasthosecausingtendril coiling (39,123)andturgorreductioninduced by water deficit (28). Mechanical impedanceduring root growthmight also induceJA accumulation,causinginhibition of root growth (113).Othermechanicalperturbations,involving wind or touch, inducechangesingrowththatmaybemediatedin partby JA. In Arabidopsisthaliana, theTCHgenesareupregulatedin responseto mechanicalperturbation(19). The TCHgenesencodecalmodulinandtwo othercalcium-binding proteins.Expressionof thesegenesincreaseswhencytoplasmic calciumlevelsrise (4). In animalcells,calciumstimulateseicosanoidbiosynthesisby activatingphospholipaseand lipoxygenase.In plant cells, similar enzymesare also involved in JAbiosynthesis, suggestingthat a similar signal transductionpathwayinvolvingcalciummay activatesynthesisof JA in responseto touchandturgor reduc-tion.

Jasmonate accumulates in response to plant wounding (29). Localizedwound-inducedJA accumulation in injuredcellscouldresultfrom themixingof compartmentsthatcontainlipases,membranesrich in LA, theprecursorof


JA, lipoxygenaseandthe otherenzymesthat areinvolved in JA biosynthesis(describedbelow).However,thesituation is morecomplexbecauseJA accu-mulationcanbeinducedin cell culturesandplantsby oligosaccharidesderivedfrom plant cell walls, by elicitors suchaschitosansderivedfrom fungal cellwalls, and by peptideinducerssuch as systemin(37, 53, 82). Thesecom-poundsare thoughtto stimulate JA biosynthesis via receptor-mediatedproc-esses.Elicitor-induced phosphorylation of a plasmalemma protein (42) andinhibition of elicitor-mediatedJA accumulationby theproteinkinaseinhibitorstaurosporin(16) are consistentwith this idea.Furthermore,wound-inducedaccumulationof JA requiresa MAP kinase(104). In someplants,ABA ap-pearsto beneededfor wound,elicitor, or systemin-mediatedJA accumulation(89). JA and JA responsivegenesalso accumulatesystemically in plantsinresponseto localizedwounding (84). The systemicsignal is apparentlyre-leasedat thewoundsiteandmigratesthroughthephloemto otherpartsof theplant. Systemin,an 18–aminoacid peptide,hasbeenshownto move in thephloem and to induce JAand JA-responsivegenes throughoutthe apicalportion of plants(84). Systeminmay be releasedfrom the wound site uponhydrolysisof a precursorpolypeptide (77). Electricalsignalshavealsobeenproposedto mediatesystemic inductionof JA in responseto wounding(124).In addition, systemicaccumulation of JA as well as transferof JA amongplantscouldoccurvia thevaporphasein theform of MeJA (43,49),althoughthe significanceof this latter pathwayunderphysiological conditions is notclear.

BIOSYNTHETIC PATHWAY AND REGULATION

The biosynthesis of jasmonatesbeginswith LA (Figure2). This fatty acid isconvertedto 13-hydroperoxylinolenic acid by lipoxygenase.13-hydroper-oxylinolenic acid is asubstratefor allene oxide synthase [alsoknown ashydroperoxide dehydratase orhydroperoxide dehydrase;seeSimpson& Gard-ner(105)]andalleneoxidecyclaseresulting intheformation of12-oxo-phyto-dienoicacid(12-oxo-PDA).Following reductionandthreestepsof betaoxida-tion, (−)-7-iso-JAis formed.Jasmonicacidcanbecatabolizedto form MeJAand numerousconjugatesand catabolitesthat may have biological activity(56). Theaccumulationof JA in plantsin responseto wounding,or treatmentwith elicitors andsystemin, canbe blockedusing inhibitors of lipoxygenase(8, 36, 41, 86). Therefore,increasesin JA level mediatedby theseinducersresultsfrom de novosynthesis rather thanreleasefrom JA conjugates.


LinolenicAcid andLipases

TheA. thaliana fad3-2fad7-2fad8mutanthasvery low levelsof linolenicacidandis unable to accumulateJA in responseto wounding (76;RA Creelman, MMcConn, J Browse & JE Mullet, unpublisheddata).Application of LA toplantsresultsin accumulationof JA (44).This indicatesthatthelevel,distribu-tion, or availability of LA coulddeterminetherateof JA biosynthesis.In onestudy, the level of free linolenic acid measuredbeforewoundingwas many

Figure 2 Biosynthetic pathway of jasmonic acid. It is postulatedthat signals (suchaselicitors)interactwith a membranereceptor, which causesthe eventual production of 13-hydroperoxyli -nolenic acid.Production of 13-hydroperoxylinolenic acid is believedto occurwith the releaseoflinolenic acidvia eithera phospholipaseor lipasefollowedby oxidation by lipoxygenase(LOX),but a preliminary oxidationof linolenic acidwhile still esterified to aphospholipid andsubsequentreleaseby a lipasecannot be ruled out. 13-hydroperoxylinolenic acidcanthenbe catabolized byhydroperoxy lyase(HL), eventually forming volatile aldehydesand traumatic acid, or via peroxy-genasepathwayto cutin monomers.Jasmonic acidarisesfrom 13-hydroperoxylinolenic acidviaanallene oxide synthase(AOS) andan alleneoxide cyclase(AOC)-dependent pathwaywith 12-oxo-phytodienoic acid (12-oxo-PDA) as an intermediate. Jasmonic acid then actsto modulategeneexpression or canbefurthercatabolized.


timeshigherthan themaximum JAaccumulated afterwounding(27).FreeLAlevelsdoubledwithin 1 h after wounding, while JA levelsrose10-fold (27).Therefore,the wound-inducedincreasein JA level could haveresultedfromreleaseof linolenic acid from phospholipids, or the utilization of LA presentbefore woundingfor JA biosynthesis.

Plant membranes,especiallychloroplastmembranes,are a rich sourceofLA esterifiedin glycerolipids andphospholipids. This hasled to the sugges-tion thatincreasesin JA couldresultfrom theactivationof phospholipasesthatreleaseLA from membranes(44).Plantextractsalsocontainhighly activeacylhydroxylasesthatcanreleasefatty acidsfrom lipids. In animalsystems,phos-pholipaseA2, activatedby micromolarlevelsof calcium,releasesarachidonicacid usedin the biosynthesis of eicosanoids.The eicosanoids, leukotrienes,andprostaglandinshavechemicalstructuressimilar to jasmonates.Thesecom-poundsmediatelocalizedstressand inflammatory responsesin animalcells.Direct evidencefor the role of a specific phospholipasein JA synthesisislacking. However, analysis of phospholipid changesand phospholipase Aactivity wasdonein tobaccocells treatedwith elicitors derivedfrom Phyto-phthoraparasitica var. nicotianae (97). Time coursestudiesshowedthat theamountof phosphatidylcholinewasreducedin responseto elicitorsandthataconcomitantincreaseof phospholipaseA activity occurred.In soybeancellculture,harpinandanextractfrom thepathogenicfungusVerticillium dahliaepromotedrapidincreasesin phospholipaseA activity (23).Uponwoundingofpotato tuber tissue, JA levels roseabout 100-fold in4 h; however,inhibitorsofanimalphospholipaseA2 (manoalideandquinacrine)did not inhibit theaccu-mulation of JA (69). PhospholipaseD, which cleavesthe headgroup fromphospholipids,couldalsotriggerreleaseof LA andstimulateJA biosynthesis.PlantphospholipaseD hasbeenidentified in plantsandis proposedto play arole inplantdefense (121).

In someinstances,fatty acidsmaybeoxidizedbeforereleasefrom lipids forJA biosynthesis.Fuessneret al (46) describethe presenceof lipoxygenase(LOX) in lipid bodieswhich oxidizesfatty acidsbeforefurther metabolism.Phospholipasespreferringoxygenatedfatty acidshavebeenobservedin sev-eral plant species(6, 9). Therefore,the oxidation of fatty acidsduring highirradiance,exposureto ozone,or as a consequenceof the oxidative burstassociatedwith plantdefense(20)maystimulatetheactivity of phospholipasesor nonspecificacyl hydrolasesresultingin releaseof oxidizedfatty acidsforJA biosynthesis.

In animalcells,arachidonicacidis deliveredto cellsfor eicosanoidbiosyn-thesisvia low density lipoproteins(54). In plants,transferof linolenic acidamongcellscouldbecarriedout by lipid transferproteinsthatarelocalizedin


theextracellularspace(114).Currentmodelspostulatethat jasmonatebiosyn-thesisis regulatedby pathogensor herbivorythroughtheproductionof elici-torsor systemicsignaling moleculesthatinteractwith receptorspresenton theplasmamembrane.The observationthat the enzymesof the JA biosyntheticpathwayareprimarily localizedin plastids (10, 17) suggeststhatmechanismsmust exist to shuttleLA releasedfrom the plasmamembraneto the plastid.Alternatively,signal perception could betransmitted toplastids forsubsequentrelease of freeLA in thatorganelle.

Lipoxygenase(LOX)

Treatmentof plantswith LOX inhibitors (8, 86) and transgenicplantswithreducedLOX activity (10) havereducedability to synthesizeJA. Therefore,LOX mediatesan essentialstep in JA biosynthesis.In animals, eicosanoidbiosynthesis is regulatedin part throughcalciumandproteinmodulatedinter-actionof LOX with membranesandits substrate(35, 79).In plants,therole ofLOX in the regulationof JA biosynthesis hasbeen difficultto analyzebecausemostplantshavenumerousgenesencodingLOX, different isoformsof LOXhavedifferentenzymespecificity,andLOX is presentin morethanonecom-partmentin plantcells (i.e.45, 64,83,100).

Plantlipoxygenases(EC 1.13.11.12) oxygenate linolenic acid atthe 9or 13positionto give9- or 13-hydroperoxylinolenic acid.The roleof 9-hydroperox-idesandtheir catabolitesin plantsis unclear(119).Theroleof LOX isozymesin the productionof hydroperoxideisomersalsoneedsfurther investigation.LOX from tendrilsof Bryoniadioica consists of a majorisoformwith pI = 6.5and minor constituents with pI = 6.7 and 7.3 (38). TheseLOX isoformsprimarily produce13-hydroperoxylinolenic acid, whereasa preparationfromcell cultures containsat leastsevenLOX isoformsin thepI rangefrom 6.3–6.7and 7.3–7.5with themajorreaction product9-hydroperoxylinolenicacid (38).

LOX isozymesare found in the plasmalemma/microsomesof cucumbercotyledons(CucumissativusL.) (81). In soybeanleaves,LOX accumulatesinthevacuolesof paraveinalmesophyllcells(52).Elsewhere,LOX is associatedwith epidermaland cortical cells and is presentin vacuolesand plastids.Inplastids,a methyl jasmonate–inducedLOX is sequesteredinto protein inclu-sion bodies(52). This may be importantin restrictingthe interactionof LOXwith fatty acids.Similarly, in barley, jasmonate–inducedLOX isozymes arelocalizedin plastids (45).

Changes inthedistribution andabundanceof LOX duringdevelopmentandin different tissues and compartmentsis due in partto the expressionofdifferent membersof the Lox genefamily. For example,two different LOX


genes,AtLox1 (78) and AtLox2 (11), have been identified in A. thaliana.AtLox1is expressed inleaves, roots,inflorescences,and youngseedlings, withthe highestexpressionfound in roots and young seedlings.BecauseAtLox1lacksobvioustargetingsequences,this enzymeis mostlikely localizedin thecytoplasm.In contrast,AtLox2 is localizedin chloroplasts(10). Thepresenceof a plastidtransitsequencesuggeststhata rice LOX thatcatalyzestheexclu-sive formation of 13-hydroperoxylinolenateis also localizedin chloroplasts(90). AtLox2 mRNA levels are high in leavesand inflorescencesbut low inseeds,roots,andstems.Thephysiologicalroleof thischloroplastlipoxygenasewasanalyzedby reducingLOX2 accumulationin transgenicplants(10). Thereductionof AtLox2 expressioncausedno obvious changesin plant growth.However,the wound-inducedaccumulationof JA observedin control plantswas absentin leavesof transgenicplants lacking LOX2. Therefore,plastidlocalized LOX2 is required for wound-inducedsynthesis of jasmonatesinArabidopsisleaves.

AlleneOxideSynthase and Other Stepsin JA Biosynthesis

Thefateof 13-hydroperoxylinolenateproducedby lipoxygenaseis anotherkeybranchpointin the jasmonatebiosyntheticpathway(Figure2). Hydroperoxidelyasewill cleave13-hydroperoxylinolenateto form volatile six carbonalde-hydesand12-oxo-dodecenoicacid (119). 13-hydroperoxylinolenatecanalsobe usedby peroxygenaseto produceprecursorsof cutin molecules (18). Incontrast,productionof jasmonatesrequiresthat 13-hydroperoxylinolenatebemetabolizedto alleneoxide by alleneoxide synthase(AOS; IUBMB namehydroperoxidedehydratase,EC 4.2.1.92).Other namespreviously usedforAOS includehydroperoxideisomerase,hydroperoxide cyclase,andfatty acidhydroperoxidedehydrase.Flax and ArabidopsisAOS havebeenclonedandcharacterized(21, 107,108; E Bell, RA Creelman& JE Mullet, unpublisheddata).Flax AOS is a 55-kDahemoproteinwith thespectralcharacteristicsof acytochromeP450anda turnoverrateof 1000min−1. TheprimarystructureofAOSdeducedfrom its cDNA revealsaproteinof 536aminoacidscontainingaC-terminaldomainhomologousto a region in many cytochromeP450sthatcontaina heme-bindingcysteine.The flax cDNA encodesa 58–aminoacidN-terminalsequencecharacteristicof chloroplasttransitpeptides.This is con-sistentwith localizationof AOS activity in chloroplasts(120).TheArabidop-sis AOS (availablefrom the Ohio StateUniversity ArabidopsisBiologicalResourceCenterasEST94J16T7,GenBankAccessionT20864)sharesa highdegreeof homologywith flax AOS and also containsa putativeN-terminalplastid targetingsequence(RA Creelman,E Bell & JE Mullet, unpublished


data).TheArabidopsis AOS geneexistsasa singlecopy,basedon analysisoftotal DNA Southernblots (E Bell, RA Creelman& JE Mullet, unpublisheddata).Allene oxide synthaseactivity hasbeenlocalizedto the plastid outerenvelopein spinach(17), but givenits putativeplastidtargetingsequenceandhigh turnover numberfurther localization studiesare warranted.

Over-expressionof flax AOS in transgenicpotatoplantsincreasedJA lev-els(57), indicating thattheamount ofAOSproteinlimitsJA biosynthesis.Thehigh turnoverrateof flax AOS (∼1000min−1) mayhelpthis enzymecompetefor substratealsousedby hydroperoxylyaseandperoxygenasedependingonthe localizationof theseenzymesandtheir substrateaccessibility.13-hydrop-eroxylinolenateproducedby a plastidlocalizedLOX maybemoreaccessibleto AOSlocalizedto plastids. Recentstudies haveshown thatAOSactivity washigherin tissueswith elevatedJA, suggesting thatdifferencesin JA thatoccurduring plant developmentmay be causedby variation in AOS abundanceoractivity (105).Similar analysisof AOS level andactivity needsto be carriedout in plantsexposedto elicitorsand systemin, orafterwounding.

Nonenzymatic cyclizationof alleneoxide will yield a racemicmixture of12-oxo-PDA.However,alleneoxide cyclase(55) catalyzesthestereospecificformationof the9S,13Senantiomerof 12-oxo-PDA.Theenzymescatalyzingreductionof 12-oxo-PDAand β-oxidation leadingto JA havebeendemon-strated invitro buthave notbeen extensivelycharacterized(119).

Thetomatomutant,JL5, is inhibitedin theconversionof 13-hydroperoxyli-nolenateto 12-oxo-PDA(60). This mutant,which couldbealteredin AOS orAOC activity, wasidentifiedby screeningplantsfor reducedlevelsof wound-inducedPin2expression.Diethyldithiocarbamicacid (DIECA),an inhibitor ofJA biosynthesis,wasshownto efficiently reduce13-hydroperoxylinolenateto13-hydroxylinolenicacid (37, 41). This suggeststhatDIECA inhibits JA bio-synthesisby reducing theprecursor poolleadingto allene oxide.Salicylicacid(SA), a mediatorof someplant defenseresponses,inhibits the conversionof13-S-hydroperoxy linolenic acid to12-oxo-PDA (37,41,87, 124).

JASMONATE SIGNAL TRANSDUCTION

The JA signal transductionpathwayis mainly unknown.It is presumedthatjasmonateinteractswith receptorsin thecell thatactivatea signaling pathwayresultingin changesin transcription,translation,andotherresponsesmediatedby JA. Lack of high specificactivity JA andthe lipophilic andvolatile natureof JA andMeJA will makedirectanalysisof JA receptorsdifficult. Jasmonatereceptorsandothercomponents of the signal transductionpathwayaremorelikely to be discoveredthrough analysisof mutantsthat are insensitive or


alteredin their responseto JA. To date,up to four differentclassesof JA-in-sensitivemutantshavebeenidentified;coi1, jar1, jin1, andjin4 (12,14,113).Geneticstudieswereunableto determinewhetherjin4 and jar1 wereallelic(14). The mutants jar1, jin1, and jin4 were recoveredusing a root growthscreen(wild type A. thaliana root growth is inhibited by 1–10 mM JA). Incontrast,coi1 wasidentifiedbecauseplantswereresistantto coronatine(47).Coronatineis a chlorosis-inducingtoxin thathasa chemicalstructure(Figure1) and biological activity similar to JA. The coi1 mutant also shows aMeJA–insensitive rootgrowthphenotype.

Application of jasmonate to plants causeslarge changesin translation,transcription,andmRNA populations(103).Treatmentof barleyleaveswithjasmonatereducedsynthesisof the largeandsmall subunits of Rubiscoandotherproteins(122).Decreasedtranslationof thelargesubunitin chloroplastswas correlatedwith a site-specificcleavagein the 5′-untranslatedportion ofthe rbcL mRNA (94,96).ThealteredrbcL mRNA 5′-endpresumablyreducesaccessto the ribosome–bindingsite locatednearthe site of translation initia-tion. Reducedsynthesisof Rubiscosmall subunit andothercytoplasmic pro-teins occurredthrough supressionof translationinitiation and reductionofmRNA levels(95).

The promotersof two jasmonate–induciblegenes,Pin2 and VspB,havebeenstudiedin somedetail (67, 74). A 50–bpdomainwas identified in thepromotersof both genesthat conferredJA responsivenesson truncatedre-portergeneconstructs.TheVspB50–bpdomaindid not confer JAresponsive-nesson a truncated−46 CaMV promoter, but induction wasobservedwhenthisDNA regionwasaddedto a−90CaMV truncatedpromoter. Thisindicatesthat factors binding to the −90 CaMV promoterwere requiredto observeJA–stimulated transcription.Both JA–responsivedomainscontain a G-boxsequence(CACGTG),which in otherpromotershasbeenshownto bind bZIPtranscriptionfactors(126). BecausebZIP protein binding sitesare found innumerous promoters that arenot responsive to JA, itis likely thatthis factor,ifit playsa role in JA mediatedresponses,interactswith other trans factorstomodulatetranscription. Mutation of the G-box in the Pin2 promoterdid notpreventJA-mediatedinduction of Pin2 (72). Jasmonateinducedaccumulationof VspBandPin2 mRNA is blockedby cycloheximide. Bestatin, an inhibitorof aminopeptidasesin plantsandanimals, inducesPin2 in the absenceof JA(101). This observationsuggeststhat induction of Pin2, and perhapsotherjasmonatemodulatedplant genes,is normally preventedby the actionof anaminopeptidase.Induction of JA–responsive genescould thereforebe medi-ated byinactivationof the proteaseor stabilization of thetarget protein.


JAFUNCTIONAND RESPONSIVEGENES

Jasmonatemodulatesthe expressionof numerousgenesand influencesspe-cific aspectsof plantgrowth,development,andresponsesto abioticandbioticstresses(seeTable1). Many of theseresponseswereidentifiedby applicationof jasmonate to plants,sometimesat nonphysiological levels.InteractionsbetweenJA andotherplantgrowthregulatorsmakeassignmentof physiologi-cal roles forJA even morecomplicated.In thesectionbelow,proposedactionsof JA in plantsarerelatedto thelevel of JA in planttissues,theactivity of JAresponsivegenes,and insightsprovidedby JA insensitive and JA deficientplants.

SeedGermination and Growth

JA andMeJA inhibit the germinationof nondormant seedsandstimulatethegerminationof dormantseeds.JA, MeJA,ABA, andethyleneinhibit germina-tion of the recalcitrantseedsof Quercusrobur (48). Whenthesedessication-sensitiveseedsweredried, the concentration ofMeJA and JAincreasedbefore

Table 1 Jasmonatefunctions andresponsive genes

PhysiologicalFunction JA ResponsiveGenes References

Seedgermination and growth

(-) seed,pollengermination ??? 47, 48, 76

(-) root growth ??? 12, 14, 113

(+) tendril coiling ??? 38, 39, 123

Photosynthesis/vegetativesinks

(-) photosynthetic apparatus (-) rbcL, rbcS 24, 94–96

(+) vegetativeprotein storage (+) Vsp,Lox 11, 15, 22, 45, 50, 52, 61,65, 73, 75, 87

(+) tuberization (+) Pin2 63, 85, 87, 88, 93

Flowerand fruit development

(+) pollenviabili ty ??? 47, 76

(+) fruit ripening, pigments (+) EFE 30, 71

(+) seeddevelopment (+) cruciferin, napin, Vsps 110, 125

Insectand diseaseresistance

(+) insectresistance (+) Pin2, othergenes 36, 37, 41, 43, 44, 49, 62

(+) diseaseresistance (+) osmotin, thionin, RIP60 9a,129

(+) Chs,Pal, HMGR, PPO,pdf, ???

25, 26, 29, 49, 82, 91


the lossin seedviability. The increasein jasmonatewascorrelatedwith lipidperoxidation,which suggeststhat the production of jasmonatemay not beregulatinggermination but ratheris a consequenceof membranedamage.Inapple, jasmonate stimulated the germinationof dormant embryosand in-creasedalkaline lipase activity (92). Lipase activation may stimulatethe mobi-lization of lipid reservesto providesugarsfor seedlinggrowth. Inhibitors oflipoxygenase-inhibitedembryogerminationandJA partially reversedinhibitoraction.The level of jasmonate in soybeanseeds12 dayspost-anthesis is low(∼0.1µg/g fresh weight),whereasin olderseeds JAlevels are higher(0.5 ng/gfreshweight) (28).12 h afterimbibition, the levelof JA increasedfivefold to 2µg/g freshweight in axes.JA levelsdeclinedwith further seedlingdevelop-ment.The observedincreasein JA levels following imbibition is correlatedwith seedreservemobilization andthereforemaybeaconsequenceratherthana trigger of germination.The jasmonate-insensitivemutants, jin4 and jar1,showincreasedsensitivity to ABA inhibition of germination (14,113).There-fore, JA may stimulate seedgerminationby decreasingsensitivity to ABA.Alternatively,JA-mediatedgrowthinhibition couldblockseed germination.

JA stronglyinhibits root growthby a mechanismnot mediatedby ethylene(14).JA alsoinhibits IAA-stimulatedcoleoptile elongationpossibly by block-ing incorporation ofglucoseinto cell wall polysaccharides(118).Furthermore,JA activatesthedifferentialgrowthinvolvedin tendril coiling, a responsethatdoesnot directly involve ethyleneor IAA (39). Furtherwork is neededtodefine therole of JA ingrowthprocesses.

VegetativeSinksandStorage Proteins

Plantshavethecapacityto accumulatelargeamountsof carbonandnitrogeninspecificcellsandtissuesandto mobilizethesematerialsfor usein otherpartsof the plant. This capacityis usedduring seedformationwhennutrientsaremovedfrom thevegetativeplant to developingseeds,andduringseedgermi-nation when carbonand nitrogen are mobilized for seedlingdevelopment.Transientstorageand mobilization of nutrientsalso occur during vegetativegrowth.For example,carbonoftenaccumulatesin chloroplasts duringthedayandis mobilized at night to otherpartsof theplant.Carbonandnitrogenmayalsoaccumulatein cells locatedin meristematic regionsfor useduring rapidcell growth.For osmotic reasons,cells areonly ableto accumulatea limi tedamountof sucroseandaminoacids.Therefore,largeamountsof carbonandnitrogenaccumulateas polymersin the formof starch,fructans, and proteins.

A role for jasmonicacidin proteinstoragein plantswassuggested,in part,becausejasmonate levelsarehighin vegetativesinks.As notedabove,jasmon-


ate levels are higherin soybeanaxes, plumules, andthe hypocotyl hookrelativeto thehypocotylzoneof cell elongation and thenonelongating portionof stemsand roots (28). In six-week-oldsoybeanseedlings, JA levels arehigherin younggrowingleavesthatareimporting carbonandnitrogenthaninolder fully expandedleaves(28). High levelsof JA arepresentin developingreproductivestructures,especiallypods,with lower levelsin seeds.Jasmonateor aderivativeof jasmonate,tuberonicacid,hasbeenproposedto playarole inthe formationof tubers,a special typeof vegetativesink (68,85, 93).

A secondreasonto suggestthat jasmonate playsan importantrole inprotein storageduring plant developmentderives from the discoverythatgenesencodingvegetativestorageproteins (VSPs) (111) are regulatedbyjasmonate(2). Vegetativestorageproteinswere first describedin soybean(127,128).TheVSPsaccumulatein thevacuolesof paraveinalmesophyll andbundlesheathcells that surroundveins in soybeanleaves(50). If podsarecontinuously removedfrom plants,theVSPsaccumulateandcanaccountforasmuchas45% of the solubleproteinin leaves(128).Otherstudiesshowedthat theVSPsaccumulatein podsandotherpartsof thedevelopingreproduc-tive structurebut not in seeds(109).This led to thesuggestionthat theVSPsrepresenttemporarydepositsof amino acids derived from disassembly ofRubiscoandother leaf proteinsthat werebeingmobilizedfor seeddevelop-ment.The observationthat jasmonateregulatesVSP accumulationwasmadeby Anderson(2, 3) whentreatingsoybeancell cultureswith this compound.Later studiesshowedthat the soybeanVSPs accumulatein soybeanaxes,hypocotyl hooks,and young developingleavesand that VspBexpressioniscorrelatedwith endogenouslevelsof JA in plants(28, 73, 75). VspBexpres-sion also increasesin young leaveswhenplantsareexposedto waterdeficit(75). This is mostlikely dueto inhibition of leaf growthbut continuedimportandstorageof carbonandnitrogenin theleaf.ThesoybeanVSPsincludetwoproteinshavinglow acid phosphataseactivity (Vspa,Vspb) (33) andlipoxy-genase(65, 115). The genesencodingtheseproteinsareregulatedin a com-plex wayby JA,sugars, phosphate,nitrogen,and auxin(34,73, 98,112).

Photosynthesis, Senescence,andAbioticStress

Application of JA to leavesdecreasesexpressionof nuclearand chloroplastgenesinvolvedin photosynthesis(22,122).JA treatmentsalsocausea lossofchlorophyll from leavesor cell cultures(122). Jasmonate’s ability to causechlorosisled to thesuggestion that this compoundplaysa role in plantsenes-cence(116).However,this suggestionis difficult to reconcilewith thefindingof high JA levels in zonesof cell division, young leaves,and reproductive


structures.Unfortunately,a completeanalysisof JA levelsin senescingleaveshasnot beencarriedout. A limi tedstudyof this questionin soybeanrevealedonly small changesin JA level in soybeanleavesduring pod fill (22). ThusalthoughJA can induce senescence-likesymptoms, therole of this hormoneinmediatingsenescenceis at presentunclear.

If jasmonate-inducedchlorosisand inhibition of genesencodingproteinsinvolved in photosynthesisare not involved in senescence,then what is thephysiological role of this JA activity? JA may inhibit thesynthesisof chloro-plastproteinsduring anearlyphaseof leaf formationwherecell division andimport of nutrientsarevery active.This is consistentwith higherlevelsof JAin young leavescomparedwith older leavesof soybean.In monocotleaves,meristematic cells are localizedto the leaf base.This regionof the leaf con-tainslittl e chlorophyll, andexpressionof genesinvolved in photosynthesisislimited. Plastidsin this developmentalstageoften containstarchgrains,andthesecellsmayaccumulate vegetativestorageproteinsbeforecell enlargementandchloroplastdevelopment. Oncecells stopdividing andbeginto elongate,chloroplastdevelopmentis initiated.If developingmonocotleavesaresimilarto soybeanhypocotyls,higherjasmonateconcentrationswill bepresentin themeristematic cells of the leaf basethanin expandingandmaturecells nearertheleafapex.If this is thecase,JA couldactto inhibit prematureaccumulationof the photosynthetic apparatusin meristematic cells of the leaf basewhilestimulatingaccumulationof carbonandnitrogenreservesneededfor latercelldevelopment.We speculatethat treatmentof excisedmatureleaveswith JAmaybe recapitulatingthis earlierphaseof development.Application of JA tomatureleavesmay drive the developmentalprogramin reverseby inhibitingexpressionof chloroplastgenesand stimulating accumulation of vegetativestorage andother proteins.

Theexpressionof manygenesinvolved in photosynthesisis higherduringplant illumination comparedto darkness.JA’s ability to inhibit expressionofgenesinvolved in photosynthesiscould lower expressionof thesegenesindarkness.If JA is distributedlike ABA in plant cells, this compoundwillaccumulatein chloroplastsin illuminatedplantsbecauseof theincreasein pHin this compartment.At night, JA accumulatedin chloroplastsduring thedaywill bereleasedinto thecytoplasm, whereit couldinhibit expressionof genesinvolvedin photosynthesis.

Theability of JA to inhibit expressionof genesinvolved in photosynthesissuggeststhat jasmonatecould help reducethe plant’s capacity for carbonassimilation underconditions of excesslight or carbon.The photosyntheticapparatusmay absorbmorelight energythancanbe usedfor photosynthesisunderconditionswherecarbonfixation exceedsthecapacityof cellsto export


or store carbon.Inhibition of genesencodingthe photosynthetic apparatusundertheseconditionswould eventuallybalanceenergyabsorbingandusingcapacities. Inthe short term,JA-mediatedinduction of vegetative storageproteinsynthesisunderconditionsof high sugaraccumulation createsa sinkfor carbonandnitrogen andreleasesphosphatefrom sugarphosphatepoolsforfurther carbon fixation.

Excess lightabsorptionalso occursin plants exposed to waterdeficit,which inducesstomatalclosure,makingplantsdeficientin CO2. Undertheseconditions, theproductsof photosyntheticelectrontransportcanno longerbeusedfor carbon fixation,and the energyharvested bythe chlorophyllantennaemust be dissipatedratherthan usedfor the formation of ATP and reducingpower.Someof theexcessenergycanbedissipatedvia thexanthophyllcycleor throughotherenergy-quenchingmechanisms(31). However,oncethe ca-pacity of thesesystemsis exceeded,membranedamagewill occur.Lipoxy-genaseandotherenzymesthatmetabolizefatty acidsmayprotectmembranesfrom damageby removingoxidized fatty acids.The lipoxygenase-mediatedgenerationof JA could, in turn, induce changesin the cell that amelioratefurtherphotochemical damage.For example,jasmonate-inducedlossof chlo-rophyll would decreasetheamountof energyabsorbedby thephotosyntheticapparatus.Theaccumulation of anthocyaninsthat is stimulatedby JA in illu-minatedplants(49) couldalsoprovidesomeprotectionfrom excessradiation.

FlowerandFruit Development

Jasmonatemight beexpectedto play a role in formationof flowers,fruit, andseedbecauseof therelativelyhigh levelsof thiscompoundin developingplantreproductivetissues.Thepresenceof jasmonateandrelatedvolatile fatty acidderivativesmay be involved in insectattractionrelatedto pollen dispersal.Otheraspectsof flower, fruit, andseeddevelopmentthatcanbemodulatedbyjasmonateincludefruit ripening,fruit carotenoidcomposition, andexpressionof genesencodingseedandvegetativestorageproteins.Jasmonate-stimulatedtomatoandapplefruit ripeningmost likely occursthroughactivationof EFEandproductionof ethylene(30). It is possible that jasmonatelevelsgraduallyincreasein developingfruit leading to enhancedsynthesisof ethyleneandsubsequentfruit ripening. Application of JA to tomato fruit inhibited theaccumulationof lycopeneandstimulatedaccumulationof β-carotene(99).Thebiochemicalbasisand physiological role of this JA-mediatedchangeneedsfurther investigation.

SoybeanVspsandA. thaliana AtVspshowhigh expressionin flowers anddevelopingfruit (15, 110).The vegetativestorageproteinsmay providetem-


porarystorageof carbonandnitrogenarriving at thereproductiveapexfor useduring rapid synthesisof seedstorageproteins.The AtVSP proteinsweremissing in flowers of coi1 mutantsthat are insensitive to JA but could beinduced bytreatmentof plants withJA (12). TheJA-deficient LA mutant ofA.thaliana alsodoesnot expressAtVspunlessplantsareprovidedwith exoge-nousJA (RA Creelman,M McConn,E Bell, J Browse& JE Mullet, unpub-lisheddata). Ovulesof theLA-deficientmutantwere viable, indicatingthat JAandexpressionof theAtVspwerenot essentialfor seedformation.Therefore,although JA may modulate expressionof genesencoding seedstorageproteins(125), JA is not essentialfor production of viable ovules inA. thaliana.However,fatty acidmutants of A. thaliana that lack LA andJA andthecoi1JA-insensitive mutant fail to produceviable pollen unlesssuppliedwith JA(76).

InsectandDiseaseResistance

JA playsanimportantrole in plant insectanddiseaseresistance.Severallinesof evidencesupportthis conclusion.First, JA accumulatesin woundedplants(29) and in plantsor cell culturestreatedwith elicitors of pathogendefense(53).Second,JA activatesgenesencodingproteaseinhibitorsthathelpprotectplantsfrom insectdamage(62). JA alsoactivatesexpressionof genesencod-ing antifungalproteinssuchasthionin (9a),osmotin (129),PDF(91), andtheribosome-inactivating protein RIP60 (24). JA modulatesexpressionof cellwall proteinssuchasPRP(29) thatmaybeinvolvedin synthesis of barrierstoinfection.Furthermore,JA induces genesinvolvedin phytoalexinbiosynthesis(Chs,Pal, HMGR) (25, 29) andphenolics (polyphenoloxidase;37) that areinvolved in plant defense.The oxylipin pathwaythat leadsto JA is also thesourceof othervolatile aldehydesandalcoholsthat function in plant defenseandwound healing.For example,the C6-aldehyde 2-hexenalcompletelyin-hibited growth of PseudomonassyringaeandE. coli (32), andC6-aldehydesandalcoholsreducedaphidfecundity(59). Thesecompounds aresynthesizedfrom 13-hydroperoxylinolenicacidvia theactionof hydroperoxylyase(Figure2). Jasmonate,wounding, andelicitorsincreasetheexpressionof lipoxygenaseandstimulatehydroperoxylyaseactivity (5, 52). This responseenhancestheability of plantsto producethesix carboncompoundsthatcontributeto plantprotection.

A third typeof evidencefor JA’s role in pestresistancecomesfrom analy-sis of plantshavingmodified levelsof JA. For example,treatmentof potatowith JA increasesresistanceto Phytophthora infestans(26). The tomatomu-tant, JL5, which is inhibitedin theconversion of13-hydroperoxylinolenicacid


to 12-oxo-PDAis moresusceptible to damageby Manducasexta(60). An A.thalianamutantdeficientin LA containsnegligibleamountsof JA andneitheraccumulatesJA nor inducesJA-responsivegeneswhenwounded.Thesemu-tantsarevery susceptible to fungalgnats(M McConn,RA Creelman,E Bell,JE Mullet & J Browse,unpublished data).Treatmentof the mutants with JArestoredfungal gnat resistance,demonstrating an essentialrole for JA inresistance.

Although a generalrole for JA in plantdefenseis now well established,thespecific way that JA is deployedrelative to other defensemechanismsinresponseto insectsandpathogensneedsfurtherinvestigation.Thecomplexityof plantdefense responsesand JA’s rolewasdemonstratedin a recentstudy oftwo genes(Pdf1.1,Pdf1.2) thatareinvolvedin fungalresistancein A. thaliana.SA, aninducerof manygenesinvolvedin responsesto pathogens,wasabletoinducePR-1butnotPdf (91).Pdfexpressionwasinducedby JA, ethylene,andoxygenradicalgeneratorssuchasparaquatandrosebengal.The A. thalianamutants,ein2 andcoi1, which areblockedin their responsesto ethyleneandMeJA, respectively,werenot alteredin pathogen-mediatedinductionof PR-1but blocked in accumulationof PDF. Theseresultshave severalimportantimplications.First, theoxidative burstthatoftenaccompaniesplant responsesto pathogensmay induceJA by producingoxidizedfatty acids.Theoxidativebursthasbeenlinked to programmedcell death(70) responsesandrepresentsoneline of plant pathogendefense.JA releasedfrom injuredcells could thenactivatefurtherdefenseresponsesincluding systemic ones.Second,this studyshowsthat pathogenssuchas A. brassicolacan trigger at leasttwo defensepathways,one involvingSA and oneinvolving JAand ethylene. This observa-tion is consistentwith reports that JA and ethylenesynergistically inducegenesthatareinvolvedin plantdefense(129).Furthermore,SA is aninhibitorof JA biosynthesisandaction(36,86).This interactionmayallow theplanttomodulatethe relativeamountof SA- andJA-inducible defensesasa functionof timeafter attack orin responseto specificpathogensor herbivores.

JA’s Dual Rolein Development andDefense

In this final section,we attemptto provide a rationalefor JA’s dual role inplant development anddefense.Thisdiscussionstartswith thefollowing ques-tions: Why aregenesencodingvegetativestorageproteinsandgenessuchasPin2 thatareinvolvedin insectdefenseregulatedsimilarly? Why arejasmon-ate-induciblegenesinvolved in plant defensealsoregulatedby sugars,phos-phate,andauxin?Why areJA levelshigh in youngapicalsinksandespeciallyreproductivestructuresbut inducibleby woundingor elicitationin olderpartsof the plant?


Theregulationof expressionof VspB,which encodesa soybeanvegetativestorageprotein,andPin2,which encodesa tomato proteaseinhibitor involvedin plant defense,is remarkablysimilar. Both genesare highly expressedinapical regionsof vegetativeplantsand in flowers and reproductivetissues.Both genesareinduceduponwoundingandapplicationof JA. Expressionofthesegenesis muchhigherwhenJA/wounding treatment occursin illuminatedplantsandinductionof geneexpressionby JA is synergistically stimulatedbysugarsandinhibited by phosphateandauxin (34, 66). The productsof thesetwo genesaretargetedto vacuoles,andlargeamountsof thetwo proteinsoftenaccumulatein plantcells.Thesimilarity of expressionof thesetwo genesandlocalizationof their geneproductssuggestthattheyplay nearlyidenticalrolesin plants,except for theactivity of theencoded proteins.

For manyreasonsit is not surprisingthat someproteinsinvolved in plantdefensealsofunction asvegetativestorageproteins.Unlike seedstoragepro-teinsthathaveto bestoredat high densityin nearlydehydratedseeds,vegeta-tive storageproteins accumulatein fully hydratedplants containing largevacuoles.Therefore,the constraints on proteinsthat serveasVSPsarefewerthan for seedstorageproteins.Plantsneedto accumulatelarge amountsofvegetativestorageproteinsandproteinsinvolvedin defensewithoutdisruptingmetabolism. Sequesteringtheseproteinsin vacuolesmayhelpaccomplishthis.Moreover,both typesof proteinsaremobilized to recoveraminoacidswhenthe needfor storageor defenseis gone.Thereforemanyproteinsinvolved inplant defense,in particularthosethat are sequesteredin vacuolesfor actionwhen ingested,are ideally suited for a role as vegetativestorageproteins.BecauseVSPsthatcanalsoaid in plantdefensehaveadditionalvaluefor theplant, perhapsmost VSPswill eventuallybe found to servea role in plantdefense.

Elevatedexpressionof JA-responsivegenessuch as Pin2 in vegetativeapices,young leaves,and reproductivestructuresmay simply be the conse-quenceof their roleasvegetativestorageproteins.However,theaccumulationof defensiveproteinsin thesetissuesalsoprovidestheplantwith a preformeddeterrentto herbivory anddiseasein regionsof the plant critical to survivaland reproduction.The differential accumulation of compoundsinvolved indefensein plant tissuesof high valueis consistentwith the “optimal defensetheory” describedby researchersworking in theareaof chemicalecology(7).This theorypredictsthatdefenseshouldbeallocatedto plantpartsthatcontrib-ute significantly to a plant’s fitnessandhavea high probability of attack.Asecondclassof chemicaldefensetheory,the“C/N theory,”emphasizesthefactthat allocationof carbonand nitrogento defensemay occur in competitionwith the useof theseresourcesfor growth anddevelopment(7). This theory


rationalizeswhy plants mayinducecarbon-richdefenses(i.e. tannins, phenols)vsnitrogen-richdefenses(i.e. proteins) depending on nutrient availability. Theinducibleor activateddefensesystemmediatedby JA is consistentwith theC/N theoryof chemicaldefensein severalways.In older leaves,JA levelsandJA-inducibledefenseis activatedin responseto woundingor elicitors, thuslimit ing the allocationof nutrientsto defenseto situations wherethis is re-quired.In addition,expressionof Pin2 is regulated notonly by the presence ofJA but also by sugars(63, 88). Dual regulationby sugarsand JA is alsoobservedin othergenessuchasChs that are involved in plant defense.Fur-thermore,Vsp expressionandperhapsgenessuchas Pin2 is inhibited whenplantsaregrownin limi ting nitrogenconditions(112).This typeof regulationwould minimize the allocationof carbonandnitrogento proteinsandsecon-dary metabolitesinvolved in plant defenseunderconditions wherenutrientsarelimiting.

CONCLUDING REMARKS

The volume of publicationsand reviewson jasmonateover the pastdecadedocumentsthe increasinginterest in this compound and its role in plants.Researchon this topic hassolidified our understanding of the chemistryandbiosynthetic pathwayof jasmonates.However,additional researchis neededinto the mechanisms thatregulatethesynthesis ofJA in plantsduring develop-ment and in responseto wounding and oligosaccharidesand peptidesthatmodulateJA biosynthesis.Transgenicplantscontaining sense/antisensecon-structsof genesin the biosynthetic pathwayandmutantsdeficientin JA willhelpprovidedefinitive information.Our understandingof theJA signaltrans-ductionpathwaywill rapidly advanceasgenesidentified throughanalysisofJA-insensitive mutants. Recentdirect evidencefor JA’s role in plant defenseconfirms this role for JA originally suggestedfrom studies of soybeancellcultures.The deploymentof JA-inducible genesaspart of the complexplantdefensesystemwill be a topic of intensefuture study. Insight gainedfromthesestudiesshould lead to betterdesignof durableplant defenseand im-provedutili zationof proteinsandgenesfrom nonplantsourcesfor plant pro-tection.

ACKNOWLEDGMENTS

We thank our colleaguesin this field for their insightful commentsand forsendingrecentpublicationsonthis topic.Becauseof lengthrestrictionsandtheavailability of otherreviews,we apologizein advancefor beingunableto citeall of theexcellentpublicationsonthis topic.Theauthors’ researchon jasmon-


atehasbeensupportedby theUSDA NationalResearchInitiative, theNationalScienceFoundation, and theTexas AgriculturalExperimentStation.

Visit the Annual Reviews home pageat http://www.annurev.org

LiteratureCited

1. AlbrechtT, KehlenA, Stahl K, Knöfel HD,SembdnerG,WeilerEW.1993.Quantifica-tionof rapid transient increasesin jasmonicacidin woundedplantsusingamonoclonalantibody. Planta 191:86–94

2. Anderson JM. 1988. Jasmonic acid-de-pendent increasesin the level of specificpolypeptides in soybeansuspension cul-turesandseedlings. J.Plant GrowthRegul.7:203–11

3. Anderson JM. 1991. Jasmonic acid–de-pendent increasein vegetativestoragepro-tein in soybean tissue culture. J. PlantGrowth Regul. 10:5–10

4. AntosiewiczDM, Polisenky DH, BraamJ.1995. Cellular localization of the Ca2+

binding TCH3 protein of Arabidopsis.Plant J. 8:623–36

5. Avdiushko S, Croft KP, Brown GC, Jack-sonDM, Hamilton-KempTR, HildebrandD. 1995. Effectof volatile methyl jasmon-ate on the oxylipin pathway in tobacco,cucumber, andArabidopsis. Plant Physiol.109:1227–30

6. Bafor M, Smith MA, Jonsson L, StobartK, Stymne S. 1993. Biosynthesisof ver-noleate (cis-12-epoxyoctadeca-cis-9-enoate) in microsomal preparations fromdeveloping endospermof Ephorbia lagas-cae.Arch.Biochem.Biophys.303:145–51

7. Baldwin IT. 1994. Chemical changesrap-idly induced by folivory. In InsectPlantInteractions, ed. EA Bernays, pp. 1–23.Boca Raton, FL: CRCPress

8. Baldwin IT, Schmelz EA, ZhangZP. 1996.Effectsof octadecanoid metabolitesandin-hibitors on inducednicotine accumulationin Nicotiana sylvestris. J. Chem.Ecol. 22:61–74

9. BanasA, JohanssonI, Stymne S. 1992.Plant microsomal phospholipasesexhibitpreference for phosphatidylcholine withoxygenated acyl groups. Plant Sci. 84:137–44

9a. Becker W, Apel K. 1992. Isolation andcharacterizationof acDNA cloneencoding

a novel jasmonate-inducedprotein of bar-ley (Hordeumvulgare L.). Plant Mol. Biol.19:1065–67

10. Bell E, CreelmanRA, Mullet JE.1995. Achloroplast lipoxygenase is required forwound-induced jasmonic acid accumula-tion in Arabidopsis. Proc. Natl. Acad. Sci.USA92:8675–79

11. Bell E, Mullet JE. 1993. Characterizationof an Arabidopsis lipoxygenasegene re-sponsive to methyl jasmonate andwound-ing. Plant Physiol. 103:1133–37

12. Benedetti CE, Xie DX, Turner JG. 1995.COI1-dependent expressionof an Arabi-dopsisvegetativestorageproteinin flowersandsiliquesandin responseto coronatineor methyl jasmonate. Plant Physiol. 109:567–72

13. BennettRN,WallsgroveRM. 1994. Secon-dary metabolites in plant defence mecha-nisms. NewPhytol. 127:617–33

14. Berger S, Bell E, Mullet JE. 1996. Twomethyl jasmonate-insensitive mutantsshow altered expressionof AtVsp in re-sponsetomethyl jasmonateandwounding.Plant Physiol. 111:525–31

15. BergerS,Bell E,SadkaA, MulletJE.1995.Arabidopsis thaliana Atvspis homologoustosoybeanVspAandVspB, genesencodingvegetative storage protein acid phos-phatasesand is regulated similarly bymethyl jasmonate,wounding, sugars,lightandphosphate. Plant Mol. Biol. 27:933–42

16. BlechertS,BrodschelmW,HölderS,Kam-merer L, Kutchan TM, et al. 1995. Theoctadecanoic pathway: signal moleculesfor the regulation of secondary pathways.Proc.Natl. Acad. Sci.USA92:4099–105

17. Blée E, Joyard J. 1996. Envelope mem-branesfrom spinachchloroplastsare asiteof themetabolismof fatty acidhydroperox-ides. Plant Physiol. 110:445–54

18. Blée E, Schuber F. 1994. Oxylipins inplants:theperoxygenasepathway. SeeRef.63a, pp. 262–64

19. BraamJ, Davis RW. 1990. Rain-, wind-,


and touch-induced expression of cal-modulin and calmodulin-related genes.Cell 60:357–64

20. Bradley DJ, Kjellbom P, Lamb CJ. 1992.Elicitor- and wound-induced oxidativecross-linking of a proline-rich plant cellwall protein: a novel, rapid defense re-sponse. Cell 70:21–30

21. BrashAR,SongWC.1995.Structure-func-tion featuresof flaxseedalleneoxide syn-thase. J. Lipid Mediat. Cell Signal 12:275–82

22. Bunker TW, Koetje DS, StephensonLC,Creelman RA, Mullet JE, Grimes HD.1995. Sink limitation inducesthe expres-sionof multiplesoybeanvegetativelipoxy-genasemRNAswhile the endogenous jas-monic acid level remains low. Plant Cell7:1319–31

23. Chandra S, HeinsteinPF, Low PS.1996.Activation of a phospholipaseA by plantdefense elicitors. Plant Physiol. 110:979–86

24. Chaudhry B, Mueller-Uri F, Cameron-Mi lls V, Gough S, SimpsonD, et al. 1994.Thebarley60kDajasmonate-inducedpro-tein (JIP60) is a novel ribosome-inactivat-ing protein. Plant J. 6:815–24

25. Choi D, BostockRM, Avdiushko S,Hilde-brand DF. 1994. Lipid-derivedsignalsthatdiscriminatewound- andpathogen-respon-sive isoprenoid pathways in plants:methyljasmonateand the fungal elicitor arachi-donic acid induce different 3-hydroxy-3-methylglutaryl-coenzyme A reductasegenes antimicrobial isoprenoids in So-lanum tuberosum L. Proc.Natl. Acad. Sci.USA91:2329–33

26. CohenY, Gisi U, NidermanT. 1993. Localand systemic protection against Phyto-phthora infestans induced in potato andtomato plants by jasmonic acid and jas-monic methyl ester. Phytopathology 83:1054–62

27. Conconi A, Miquel M, BrowseJA, RyanCA. 1996. Intracellular levels of free li -nolenic and linoleic acids increasein to-matoleavesin responsetowounding. PlantPhysiol. 111:797–803

28. CreelmanRA, Mullet JE.1995. Jasmonicaciddistributionandactionin plants:Regu-lation duringdevelopment andresponsetobiotic andabiotic stress. Proc. Natl. Acad.Sci. USA92:4114–19

29. Creelman RA, Tierney ML, Mullet JE.1992. Jasmonic acid/methyl jasmonateac-cumulate in woundedsoybeanhypocotylsand modulate wound gene expression.Proc.Natl. Acad. Sci. USA89:4938–41

30. Czapski J,SaniewskiM. 1992. Stimulation

of ethylene productionandethylene-form-ingenzymein fruitsof thenon-ripeningnorandrin tomatomutants by methyl jasmon-ate. J. Plant Physiol. 139:265–68

31. Demmig-AdamsB, AdamsWW III. 1992.Photoprotection and other responses ofplantsto highlight stress. Annu.Rev. PlantPhysiol. Plant Mol. Biol. 43:599–626

32. DengW, Hamilton-KempTR, NielsenMT,AndersenRA, Coll insGB,HildebrandDF.1993. Effectsof six-carbon aldehydesandalcoholsonbacterialproli feration. J.Agric.Food Chem.41:506–10

33. DeWald DB, MasonHS,Mullet JE.1992.The soybean vegetative storage proteinsVSPa andVSPbare acidphosphatasesac-tiveonpolyphosphates. J.Biol. Chem.267:15958–64

34. DeWald DB, Sadka A, Mullet JE. 1994.Sucrosemodulation of soybeanVspgeneexpression is inhibited by auxin. PlantPhysiol. 104:439–44

35. Dixon RAF, Diehl RE, OpasE, Rands E,VickersPJ,et al. 1990. Requirement of a5-lipoxygeanse-activating proteinfor leuk-otriene synthesis. Nature343:282–84

36. DoaresSH, Narvaez-Vasquez J, ConconiA, Ryan CA. 1995. Salicylic acid inhibitssynthesisof proteinaseinhibitorsin tomatoleavesinducedby systemin andjasmonicacid. Plant Physiol. 108:1741–46

37. DoaresSH, SyrovetsT, Weiler EW, RyanCA. 1995. Oligogalacturonides and chi-tosan activate plant defensive genesthrough the octadecanoid pathway. Proc.Natl. Acad. Sci. USA92:4095–98

38. Ehret R, Schab J, Weiler EW. 1994.Lipoxygenasesin Bryonia dioicaJacq.ten-drils and cell cultures. J. Plant Physiol.144:175–82

39. FalkensteinE,GrothB, MithoferA, WeilerEW. 1991. Methyljasmonate and a-li-nolenic acidarepotent inducersof tendrilcoiling. Planta 185:316–22

40. FarmerEE. 1994. Fatty acidsignalling inplants and their associated microorgan-isms. Plant Mol. Biol. 26:1423–37

41. FarmerEE,CaldelariD, PearceG,Walker-Simmons MK, Ryan CA. 1994.Diethyldithiocarbamic acidinhibits theoc-tadecanoid signaling pathway for thewoundinductionof proteinaseinhibitorsintomatoleaves. Plant Physiol. 106:337–42

42. FarmerEE, PearceG, RyanCA. 1989. Invitro phosphorylation of plant plasmamembrane proteinsin responseto the pro-teinase inhibitor inducing factor. Proc.Natl. Acad. Sci. USA86:1539–42

43. Farmer EE, Ryan CA. 1990. Interplantcommunication: airborne methyl jasmon-


ateinducessynthesis of proteinaseinhibi-tors in plant leaves. Proc. Natl. Acad. Sci.USA87:7713–16

44. FarmerEE,RyanCA. 1992. Octadecanoidprecursors of jasmonic acid activate thesynthesis of wound-inducible proteinaseinhibitors. Plant Cell 4:129–34

45. FeussnerI, HauseB, Voros K, Parthier B,WasternackC. 1995. Jasmonate-inducedlipoxygeanseformsarelocalizedin chloro-plastof barley leaves(Hordeumvulgarecv.Salome). Plant J. 7:949–57

46. FeussnerI, WasternackC, Kindl H, KuhnH. 1995. Lipoxygenase-catalyzed oxy-genation of storagelipids is implicatedinlipid mobil ization during germination.Proc.Natl. Acad. Sci. USA92:11849–53

47. Feys BJF, Benedetti CE, Penfold CN,Turner JG.1994. Arabidopsis mutants se-lectedfor resistancetothephytotoxin coro-natine are male sterile, insensitive tomethyl jasmonate,andresistantto abacte-rial pathogen. Plant Cell 6:751–59

48. Finch-SavageWE, Blake PS, Clay HA.1996. Desiccation stress in recalcitrantQuercusrobur L seedsresults in lipid per-oxidation and increasedsynthesisof jas-monatesandabscisic acid. J. Exp.Bot. 47:661–67

49. Franceschi VR, GrimesHD. 1991. Induc-tionof soybeanvegetativestorageproteinsandanthocyaninsbylow-levelatmosphericmethyl jasmonate. Proc. Natl. Acad. Sci.USA83:6745–49

50. Franceschi VR, WittenbachVA, GiaquintaRT. 1983.Paraveinalmesophyll of soybeanleaves inrelation to assimilatetransferandcompartmentation. Plant Physiol. 72:586–89

51. Gardner HW. 1995. Biological roles andbiochemistry of thelipoxygenasepathway.HortScience30:197–205

52. GrimesHD, Koetje DS, FranceschiVR.1992. Expression, activity, andcellularac-cumulation of methyl jasmonate-respon-sive lipoxygenase in soybean seedlings.Plant Physiol. 100:433–43

53. Gundlach H, Müller MJ, Kutchan TM,ZenkMH. 1992. Jasmonic acidis a signaltransducerin elicitor-inducedplantcellcul-tures. Proc. Natl. Acad. Sci. USA 89:2389–93

54. Habenicht AJR,Salbach P, Goerig M, ZehW, Janssen-Timmen U, et al. 1990. TheLDL receptor pathway delivers arachi-donic acidfor eicosanoid formationin cellsstimulatedby platelet-derivedgrowth fac-tor. Nature345:634–36

55. Hamberg M, Fahlstadius P. 1990. All eneoxide cyclase:a newenzymein plantlipid

metabolism. Biochem.Biophys.Acta276:518–26

56. Hamberg M, GardnerHW. 1992. Oxylipinpathway to jasmonates:biochemistry andbiological significance. Biochim. Biophys.Acta1165:1–18

57. Harms K, Atzorn R, Brash A, Kühn H,Wasternack C, Wil lmitzer L, Peña-CortésH. 1995. Expression of a flax alleneoxidesynthasecDNA leadsto increasedendo-genous jasmonic acid(JA) levels in trans-genic potato plantsbut not toacorrespond-ing activation of JA-Responding Genes.Plant Cell 7:1645–54

58. HeilmannB,HartungW,GimmlerH.1980.The distribution of abscisic acid betweenchloroplastsandcytoplasmof leafcellsandthe permeability of the chloroplast enve-lope for abscisic acid. Z. Pflanzenphysiol.97:67–78

59. HildebrandDF, Brown GC, JacksonDM,Hamilton-KempTR.1993. Effectsof someleaf-emitted volatile compounds on aphidpopulation increase. J. Chem.Ecol. 19:1875–87

60. HoweGA, LightnerJ,BrowseJ,RyanCA.1996. An octadecanoid pathway mutant(JL5) of tomato iscompromisedin signal-lingfor defenseagainstinsectattack. PlantCell. In press

61. HuangJ-F, Bantroch DJ, Greenwood JS,Staswick PE. 1991. Methyl jasmonatetreatment eliminatescell-specific expres-sionof vegetative storageprotein genesinsoybeanleaves. Plant Physiol. 97:1512–20

62. Johnson R, NarvaezJ, An GH, Ryan C.1989. Expression of proteinaseinhibitors IandII in transgenic tobacco plants: effectson natural defenseagainstManduca sextalarvae. Proc. Natl. Acad. Sci. USA 86:9871–75

63. JohnsonR,RyanCA. 1990. Wound-induc-ible potato inhibitor II genes:enhancementof expression by sucrose. Plant Mol. Biol.14:527–36

63a. Kader J-C, ed. 1994. Plant Lipid Metabo-lism.Dordrecht: Kluwer

64. KatoT,OhtaH,TanakaK, ShibataD.1992.Appearanceof new lipoxygenasesin soy-beancotyledonsaftergermination andevi-dencefor expressionof amajor newlipoxy-genasegene. Plant Physiol. 98:324–30

65. Kato T, Shirano Y, Iwamoto H, Shibata D.1993. SoybeanlipoxygenaseL-4,acompo-nentof the94-kilodalton storageprotein invegetativetissues:expressionandaccumu-lationin leavesinducedbypodremovalandby methyl jasmonate. Plant Cell Physiol.34:1063–72

66. Kernan A, Thornburg RW. 1989. Auxin


levelsregulate the expression of awound-inducible proteinaseinhibitor II-chloram-phenicol acetyl transferasegene fusion invitro andin vivo. Plant Physiol. 91:73–78

67. Kim SR,Choi JL,CostaMA, An GH.1992.Identification of a G-box sequenceas anessential elementfor methyl jasmonate re-sponseof potatoproteinaseinhibitor II pro-moter. Plant Physiol. 99:627–31

68. Koda Y. 1992. The role of jasmonic acidandrelatedcompounds in theregulation ofplant development. Int. Rev. Cytol. 135:155–99

69. Koda Y, Kikuta Y. 1994. Wound-inducedaccumulationof jasmonic acidin tissuesofpotato tubers. Plant Cell Physiol. 35:751–56

70. Korsmeyer SJ.1995. Regulators of celldeath. Trends Genet. 11:101–5

71. LopezR,DatheW, BrucknerC,MierschO,SembdnerG.1987. Jasmonicacidin differ-ent parts of the developing soybeanfruit.Biochem. Physiol. Pflanzenphysiol. 182:195–201

72. Lorbeth R,DammannC,EbnethM, AmatiS,Sanchez-SerranoJJ.1992. Promoterele-ments involved in environmentalandde-velopmental control of potato proteinaseinhibitor II expression. Plant J. 2:477–86

73. Mason HS, DeWald DB, CreelmanRA,Mullet JE.1992. Coregulation of soybeanvegetativestorage proteingene expressionby methyl jasmonateand soluble sugars.Plant Physiol. 98:859–67

74. MasonHS,DeWald DB, Mullet JE.1993.Identification Of a methyl jasmonate-re-sponsive domainIn the soybeanvspBpro-moter. Plant Cell 5:241–51

75. MasonHS,Mullet JE.1990. Expression oftwo soybean vegetative storage proteingenes during developmentandin responseto water deficit, wounding, and jasmonicacid. Plant Cell 2:569–79

76. McConn M, BrowseJ. 1996. The criticalrequirement for linolenic acidis pollende-velopment,not photosynthesis,in anArabi-dopsis mutant. Plant Cell 8:403–16

77. McGurl B, Ryan CA.1992. The organiza-tion of the prosystemin gene. Plant Mol.Biol. 20:405–9

78. MelanMA, Dong XH, EndaraME, DavisKR, Ausubel FM, PetermanTK. 1993. AnArabidopsis thaliana lipoxygenase genecanbeinducedbypathogens,abscisicacid,and methyl jasmonate. Plant Physiol.101:441–50

79. Mi ller DK, Gillard JW, Vickers PJ,Sadowski S,LéveilleC,etal.1990. Identi-fication andisolation of a membrane pro-

tein necessaryfor leukotrieneproduction.Nature343:278–81

79a. MooreTS,ed. 1993. Lipid MetabolisminPlants.BocaRaton, FL: CRC Press

80. Mueller MJ,Brodschelm W. 1994. Quanti-fication of jasmonic acid by capillary gaschromatography-negativechemicalioniza-tion-mass spectrometry. Anal. Biochem.218:425–35

81. Nellen A, Rojahn B, Kindl H. 1995.Lipoxygenaseforms locatedat the plantplasmamembrane. Z. Naturforsch. Teil C50:29–36

82. Nojiri H, Sugimori M, Yamane H,Nishimura Y, YamadaA, et al. 1996. In-volvementof jasmonic acid in elicitor-in-duced phytoalexin production in suspen-sion-culturedricecells. PlantPhysiol. 110:387–92

83. Park TK, Polacco JC. 1989. Distinctlipoxygenasespeciesappear in the hypo-cotyl/radicleof germinatingsoybean.PlantPhysiol. 90:285–90

84. PearceG,StrydomD,JohnsonS,RyanCA.1991. A polypeptide from tomato leavesinduces wound-inducible proteinase in-hibitor proteins. Science253:895–98

85. PelachoAM, Mingo-CastelAM. 1991.Jas-monic acid inducestuberization of potatostolonsculturedin vitro. Plant Physiol. 97:1253–55

86. Peña-CortésH, AlbrechtT, PratS, WeilerEW, Wil lmitzerL. 1993. Aspirin preventswound-inducedgeneexpression in tomatoleavesby blocking jasmonic acid biosyn-thesis. Planta 191:123–28

87. Peña-Cortés H, Fisahn J, Wil lmitzer L.1995. Signals involved in wound-inducedproteinaseinhibitor II gene expressionintomatoandpotatoplants. Proc.Natl. Acad.Sci.USA92:4106–13

88. Peña-CortésH,LiuXJ,SerranoJS,SchmidR, Wil lmitzer L. 1992. Factors affectinggeneexpressionof patatin andproteinase-inhibitor-II genefamilies in detached po-tato leaves: implications for their co-ex-pression in developing tubers. Planta 186:495–502

89. Peña-Cortés H, Wil lmitzer L. 1995. Therole of hormonesin gene activation in re-sponse to wounding. In Plant Hormones,ed. PJ Davies, pp. 395–414. Dordrecht:Klewer

90. PengY-L, Shirano Y, Ohta H, Hibino T,TanakaK, ShibataD.1994.A novel lipoxy-genasefrom rice: primary structure andspecific expression upon incompatible in-fection with rice blast fungus. J. Biol.Chem.269:3755–61

91. Penninckx IAMA, Eggermont K, Terras


FRG,ThommaBPHJ,De SamblanxGW,etal. 1996. Pathogen-inducedsystemicac-tivation of a plant defensegene in Arabi-dopsisfollowsasalicylicacid–independentpathway involving componentsof the eth-yleneand jasmonic acid responses. PlantCell. In press

92. Ranjan R, Lewak S. 1992. Jasmonic acidpromotesgerminationandlipaseactivity Innonstratified apple embryos. Physiol.Plant. 86:335–39

93. Ravnikar M, Vilhar B, Gogala N. 1992.Stimulatory effects of jasmonic acid onpotato stemnode andprotoplastculture. J.Plant Growth Regul. 11:29–33

94. Reinbothe S, Reinbothe C, Heintzen C,SeidenbecherC,ParthierB.1993.A methyljasmonate-inducedshift in thelengthof the5′ untranslatedregionimpairstranslationoftheplastidrbcL transcript in barley. EMBOJ. 12:1505–12

95. Reinbothe S, Reinbothe C, Parthier B.1993. Methyl jasmonate repressestransla-tion initiation of a specific setof mRNAsin barley. Plant J. 4:459–67

96. Reinbothe S, Reinbothe C, Parthier B.1993. Methyl jasmonate-regulatedtransla-tion of nuclear-encoded chloroplast pro-teins in barley (Hordeum vulgare L. cv.salome). J. Biol. Chem.268:10606–11

97. Roy S, PouenatML, Caumont C, CarivenC, Prevost MC, Esquerre-Tugaye MT.1995. Phospholipase activity and phos-pholipid patterns in tobaccocells treatedwith fungal elicitor. Plant Sci. 107:17–25

98. SadkaA, DewaldDB, MayGD,ParkWD,Mullet JE. 1994. Phosphate modulatestranscription of soybeanVspB and othersugar-inducible genes. Plant Cell 6:737–49

99. SaniewskiM, Czapski J. 1983. Theeffectof methyl jasmonateon lycopeneand β-caroteneaccumulation in ripening red to-mato. Experientia 39:1373–74

100.Saravitz DM, Siedow JN. 1995. Thelipoxygenase isozymesin soybean[Gly-cinemax(L.) Merr. ] leaves. Plant Physiol.107:535–43

101.Schaller A, Bergey DR, Ryan CA. 1995.Induction of wound responsegenesin to-mato leavesby bestatin, an inhibitor ofaminopeptidases. Plant Cell 7:1893–98

102.Schmidt J,Kramell R, Schneider G. 1995.Liquid chromatography electrospray tan-demmassspectrometry of amino acidcon-jugatesof jasmonic acidunderpositiveandnegative ionisation. Eur. MassSpectrom.1:573–81

103.Sembdner G, Parthier B. 1993. The bio-chemistry and the physiological and mo-

lecular actions of jasmonates. Annu. Rev.Plant Physiol. Plant Mol. Biol. 44:569–89

104.SeoS, Okamoto M, Seto H, Ishizuka K,SanoH, OhashiY. 1995. TobaccoMAPkinase:A possible mediator in wound sig-nal transduction pathways. Science270:1988–92

105.SimpsonTD, Gardner HW. 1995. All eneoxide synthaseand alleneoxide cyclase,enzymes ofthe jasmonic acidpathway, lo-calized in Glycine max tissues. PlantPhysiol. 108:199–202

106.Smith CJ. 1996. Accumulation of phy-toalexins: defencemechanismsandstimu-lus response.NewPhytol. 132:1–45

107.SongWC, BrashAR. 1991. Purifi cationofanalleneoxide synthaseandidentifi cationof theenzymeasacytochromeP-450. Sci-ence253:781–84

108.SongWC, Funk CD,BrashAR. 1993. Mo-lecularcloningof analleneoxidesynthase:acytochromeP450specializedfor theme-tabolism of fatty acid hydroperoxides.Proc.Natl. Acad. Sci. USA90:8519–23

109.StaswickPE.1989. Developmental regula-tion and the influenceof plant sinks onvegetative storageproteingene expressionin soybean leaves. Plant Physiol. 89:309–15

110.StaswickPE.1989. Preferential lossof anabundant storage protein from soybeanpods during seed development. PlantPhysiol. 90:1252–55

111.Staswick PE. 1994. Storage proteins ofvegetative plant tissues. Annu. Rev. PlantPhysiol. Plant Mol. Biol. 45:303–22

112.Staswick PE, Huang J-F, RheeY. 1991.Nitrogenandmethyl jasmonateinductionof soybean vegetative storage proteingenes. Plant Physiol. 96:130–36

113.Staswick PE,Su W, Howell SH. 1992.Methyl jasmonateinhibitionof root growthand induction of a leaf protein arede-creasedin anArabidopsisthalianamutant.Proc.Natl. Acad. Sci. USA89:6837–40

114.Sterk P, Booij H, Schellekens GA, VanKammenA, De VriesSC.1991. Cell-spe-cific expressionof the carrot EP2 lipidtransferprotein gene. Plant Cell 3:907–21

115.TranbargerTJ,FranceschiVR, HildebrandDF, GrimesHD. 1991. The soybean94-kilodalton vegetative storageprotein is alipoxygenasethatis localizedin paravienalmesophyll cell vacuoles. Plant Cell 3:973–87

116.UedaJ, Kato J, YamaneH, TakahashiN.1981. Inhibitoryeffectof methyl jasmonateand its related compounds on kinetin-in-duced retardation of oat leaf senescence.Physiol. Plant. 52:305–9


117.UedaJ, Miyamoto K, KamisakaS. 1994.Separation of a new type of plant growthregulator, jasmonates,by chromatographicprocedures. J. Chromatogr. 658:129–42

118.UedaJ, Miyamoto K, KamisakaS. 1995.Inhibitionof thesynthesisof cellwall poly-saccharides in oat coleoptile segments byjasmonic acid: relevanceto itsgrowth inhi-bition. J. Plant Growth Regul. 14:69–76

119.Vick BA. 1993. Oxygenatedfatty acidsofthe lipoxygenasepathway. SeeRef. 79a,pp. 167–91

120.Vick BA. 1994. Temporal andorgan-spe-cific expression of enzymesof fatty acidhydroperoxide metabolism in developingsunflower seedlings. See Ref. 63a, pp.280–82

121.Wang X. 1993. Phospholipases.SeeRef.79a,pp. 505–25

122.WeidhaseRAE, KramellHM, Lehmann J,Liebisch HW, Lerbs W, Parthier B. 1987.Methyljasmonate-induced changes in thepolypeptidepatternof senescingbarleyleafsegments. Plant Sci. 51:177–86

123.Weiler EW, AlbrechtT, Groth B, Xia ZQ,Luxem M, et al. 1993. Evidencefor theinvolvementof jasmonates and their oc-tadecanoid precursors in thetendril coiling

responseof Bryonia dioica. Phytochemis-try 32:591–600

124.Wildon DC,ThainJF, MinchinPEH,GubbIR, Reilly AJ,etal.1992. Electrical signal-ling and systemic proteinaseinhibitor in-duction in the wounded plant. Nature 360:62–65

125.Wilen RW, Rooijen GJH, PearceDW,Pharis RP, Holbrook LA, Moloney MM.1991. Effectsof jasmonic acidonembryo-specific processesin BrassicaandLinumoilseeds. Plant Physiol. 95:399–405

126.Wil liamsME, Foster R, Chua NH. 1992.Sequencesflanking the hexamericG-boxcoreCACGTGaffectthespecifici ty of pro-teinbinding. Plant Cell 4:485–96

127.Wittenbach VA. 1982. Effect of pod re-moval on leaf senescencein soybeans.Plant Physiol. 70:1544–48

128.Wittenbach VA. 1983. Purifi cation andcharacterization of a soybeanleaf storageglycoprotein. Plant Physiol. 73:125–29

129.Xu Y, ChangPFL,Liu D, NarasimhanML,RaghothamaKG, etal.1994. Plantdefensegenesaresynergistically inducedby ethyl-eneand methyl jasmonate. Plant Cell 6:1077–85


biosynthesisandactionof jasmonates in plants · walls, and by peptide inducers such as systemin...

Documents