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Journal of Plant Growth Regulation

, Volume 23, Issue 3, pp 223–237 | Cite as

Jasmonates as Signals in the Wound Response

  • Gregg A. Howe
Article

Abstract

Plant responses to wounding and herbivore attack are orchestrated by complex signaling pathways that link the production of chemical and physical signals at the wound site to activation of gene expression and other cellular processes. The systemic nature of many wound-induced responses provides an attractive opportunity to study intercellular signaling pathways that operate over long distances within the plant. Genetic dissection of the wound-response pathway in tomato indicates that (1) systemin and its precursor protein, prosystemin, are upstream components of an intercellular signaling cascade that requires the biosynthesis and action of jasmonic acid (JA); and (2) physiological processes regulated by this pathway confer host resistance to a broad spectrum of plant invaders. Grafting experiments conducted with mutants defective in systemic wound signaling indicate that systemin functions at or near the wound site to trigger the production of JA, which in turn acts non-cell autonomously to promote systemic defense responses. The location of JA biosynthetic enzymes within the companion cell-sieve element complex of vascular bundles, together with the accumulation of JA in vascular tissues, support a role for jasmonates as phloem-mobile signals. The recent discovery of enzymes involved in the metabolism of JA to volatile methyl-JA and bioactive JA-amino acid conjugates has potential implications for the mechanism by which JA promotes wound signaling. Species-specific differences in the mechanism of wound signaling appear to reflect the way in which the wound-induced jasmonate pathway is regulated by other signals including systemin, cell wall-derived oligosaccharides, ethylene, and insect-derived elicitors. Adding to the complexity of the wound-induced jasmonate cascade are wound-signaling pathways that operate independently of JA.

Keywords

Jasmonic acid Systemin Wound response Long-distance signaling Plant defense 

Notes

Acknowledgements

I am grateful to Dr. Gyu In Lee for critital reading of the manuscript. Research in my laboratory is supported by grants from the National Institutes of Health (R01GM57795), the U.S. Department of Energy (DE-FG02-91ER20021), the Michigan Life Sciences Corridor (085P1000466), and the Michigan Agricultural Experiment Station at MSU.

References

  1. Aldington, S, McDougall, GJ, Fry, SC 1991Structure-activity relationships of biologically active oligosaccharidesPlant Cell Environ14625636Google Scholar
  2. Berger, S 2002Jasmonate-related mutants of Arabidopsis as tools for studying stress signalingPlanta214497504PubMedGoogle Scholar
  3. Bergey, DR, Howe, GA, Ryan, CA 1996Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animalsProc Natl Acad Sci USA931205312058CrossRefPubMedGoogle Scholar
  4. Bergey, DR, Orozco-Cárdenas, ML, Moura, DS, Ryan, CA 1999A wound- and systemin-inducible polygalacturonase in tomato leavesProc Natl Acad Sci USA9617561760PubMedGoogle Scholar
  5. Birkenmeirer, GF, Ryan, CA 1998Wound signaling in tomato plants. Evidence that aba is not a primary signal for defense gene activationPlant Physiol117687693PubMedGoogle Scholar
  6. Carrera, E, Prat, S 1998Expression of the Arabidopsis abil-1 mutant allele inhibits proteinase inhibitor wound-induction in tomatoPlant J15765771PubMedGoogle Scholar
  7. Chang, CC, Ball, L, Fryer, MJ, Baker, NR, Karpinski, S, Mullineaux, PM 2004Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated-with changes in photosynthesisPlant J38499511PubMedGoogle Scholar
  8. Constabel, CP, Yip, L, Ryan, CA 1998Prosystemin from potato, black nightshade, and bell pepper: primary structure and biological activity of predicted systemin polypeptidesPlant Mol Biol365562PubMedGoogle Scholar
  9. Davis, JM, Gordon, MP, Smit, BA 1991Assimilate movement dictates remote sites of wound-induced gene expression in poplar leavesProc Natl Acad Sci USA8823932396PubMedGoogle Scholar
  10. Devoto, A, Nieto-Rostro, M, Xie, D, Ellis, C, Harmston, R, Patrick, E, Davis, J, Sherratt, L, Coleman, M, Turner, JG 2002COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in ArabidopsisPlant J32457466PubMedGoogle Scholar
  11. Doares, SH, Syrovets, T, Weiler, EW, Ryan, CA 1995Oligogalacturonides and chitosan activate plant defense genes through the octadecanoid pathwayProc Natl Acad Sci USA9240954098PubMedGoogle Scholar
  12. Ellis, C, Karafyllidis, I, Wasternack, C, Turner, JG 2002The Arabidopsis mutant cevl links cell wall signaling to jasmonate and ethylene responsesPlant Cell1415571566PubMedGoogle Scholar
  13. Engelberth, J, Alborn, HT, Schmelz, EA, Tumlinson, JH 2004Airborne signals prime plants against insect herbivore attackProc Natl Acad Sci USA10117811785Google Scholar
  14. Farmer, EE, Ryan, CA 1990Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leavesProc Natl Acad Sci USA8777137718PubMedGoogle Scholar
  15. Farmer, EE, Ryan, CA 1992Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitorsPlant Cell4129134PubMedGoogle Scholar
  16. Farmer, EE, Johnson, RR, Ryan, CA 1992Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acidPlant Physiol989951002Google Scholar
  17. Farmer, EE, Almeras, E, Krishnamurthy, V 2003Jasmonates and related oxylipins in plant responses to pathogenesis and herbivoryCurr Opin Plant Biol6372378CrossRefPubMedGoogle Scholar
  18. Gatehouse, JA 2002Plant resistance towards insect herbivores: a dynamic interactionNew Phytol156145169Google Scholar
  19. Graham, JS, Hall, G, Pearce, G, Ryan, CA 1986Regulation of synthesis of proteinase inhibitors I and II mRNAs in leaves of wounded tomato plantsPlanta169399405Google Scholar
  20. Green, TR, Ryan, CA 1972Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insectsScience175776777Google Scholar
  21. Gross, N, Wasternack, C, Köck, M 2004Wound-induced RNaseLE expression is jasmonate and systemin independent and occurs only locally in tomato (Lycopersicon esculentum cvLukullus). Phytochemistry6513431350PubMedGoogle Scholar
  22. Halitschke, R, Schittko, U, Pohnert, G, Boland, W, Baldwin, IT 2001Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responsesPlant Physiol125711717PubMedGoogle Scholar
  23. Hawkes, V, Turner, J 2004How are signalling pathways involving jasmonate and calcium linked to the wound response in ArabidopsisInternational Conference on Arabidopsis Research..(abstract) T08–002Google Scholar
  24. Hause, B, Stenzel, I, Miersch, O, Maucher-H, , Kramell, R, Ziegler, J, Wasternack, C 2000Tissue-specific oxylipin signature of tomato flowers: allene oxide cyclase is highly expressed in distinct flower organs and vascular bundlesPlant J24113126PubMedGoogle Scholar
  25. Hause, B, Hause, G, Kutter, C, Miersch, O, Wasternack, C 2003Enzymes of jasmonate biosynthesis occur in tomato sieve elementsPlant Cell Physiol44643648PubMedGoogle Scholar
  26. Herde, O, Atzorn, R, Fisahn, J, Wasternack, C, Willmitzer, L, Peña-Cortés, H 1996Localized wounding by heat initiates the accumulation of proteinase inhibitor II in abscisic acid-deficient plants by triggering jasmonic acid biosynthesisPlant Physiol112853860PubMedGoogle Scholar
  27. Herde, O, Cortes, HP, Wasternack, C, Willmitzer, L, Fisahn,  1999Electric signaling and Pin2 gene expression on different abiotic stimuli depend on a distinct threshold level of endogenous abscisic acid in several abscisic acid-deficient tomato mutantsPlant Physiol119213218PubMedGoogle Scholar
  28. Hildmann, T, Ebneth, M, Peña-Cortés, H, Sanchez-Serrano, JJ, Willmitzer, L, Prat, S 1992General roles of abscisic and jasmonic acids in gene activation as a result of mechanical woundingPlant Cell411571170CrossRefPubMedGoogle Scholar
  29. Hiraga, S, Ito, H, Sasaki, K, Yamakawa, H 2000Wound-induced expression of a tobacco peroxidase is not enhanced by ethephon and suppressed by methyl jasmonate and coronatinePlant Cell Physiol41165170PubMedGoogle Scholar
  30. Howe, GA, Ryan, CA 1999Suppressors of systemin signaling identify genes in the tomato wound response pathwayGenetics15314111421PubMedGoogle Scholar
  31. Howe, GA, Lightner, J, Browse, J, Ryan, CA 1996An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attackPlant Cell820672077CrossRefPubMedGoogle Scholar
  32. Howe, GA, Lee, GI, Itoh, A, Li, L, DeRocher, A 2000Cytochrome P450-dependent metabolism of oxylipins: cloning and expression of allene oxide synthase and fatty acid hydroperoxide lyase from tomatoPlant Physiol123711724PubMedGoogle Scholar
  33. Hudgins, JW, Franceschi, VR 2004Methyl jasmonate-induced ethylene production is responsible for conifer phloem defense responses and reprogramming of stem cambialzone, for traumatic resin duct formationPlant Physiol13521342149PubMedGoogle Scholar
  34. Jacinto, T, McGurl, B, Franceschi, V, Delano-Freier, J, Ryan, CA 1997Tomato prosystemin promoter confers wound-inducible, vascular bundle-specific expression of the β-glucuronidase gene in transgenic tomato plantsPlanta203406412Google Scholar
  35. Karban, R, Baldwin, IT. 1997Induced response to herbivoryChicago University PressChicagoGoogle Scholar
  36. Kennedy, GG 2002Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon.Annu Rev Entomol485172Google Scholar
  37. Kessler, A, Baldwin, IT 2002Plant responses to insect herbivory: the emerging molecular analysisAnnu Rev Plant Biol53299328PubMedGoogle Scholar
  38. Kessler, A, Halitschke, R, Baldwin, IT 2004Silencing the jasmonate cascade: Induced plant defenses and insect populationsScience305665668PubMedGoogle Scholar
  39. Korth, KL 2003Profiling the response of plants to herbivorous insectsGenome Biol4221PubMedGoogle Scholar
  40. Kubigsteltig, I, Laudert, D, Weiler, EW 1999Structure and regulation of the Arabidopsis thaliana allene oxide synthase genePlanta208463471PubMedGoogle Scholar
  41. Kumar, D, Klessig, DF 2003High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activityProc Natl Acad Sci USA1001610116106PubMedGoogle Scholar
  42. Kunkel, BN, Brooks, DM 2002Cross talk between signaling pathways in pathogen defenseCurr Opin Plant Biol5325331CrossRefPubMedGoogle Scholar
  43. Landgraf, P, Feussner, I, Hunger, A, Scheel, D, Rosahl, S 2002Systemic accumulation of 12-oxo-phytodienoic acid in SAR-induced potato plantsEurep J Plant Pathol108279283Google Scholar
  44. LeBrasseur, ND, Macintosh, GC, Perez-Amador, MA, Saitoh, M, Green, PJ 2002Local and systemic wound-induction of RNase and nuclease activities in Arabidopsis: RNS1 as a marker for a JA-independent systemic signaling pathwayPlant J29393403PubMedGoogle Scholar
  45. Lee, GI, Howe, GA 2003The tomato mutant spr1 is defective in systemin perception and the production of a systemic wound signal for defense gene expressionPlant J33567576PubMedGoogle Scholar
  46. León, J, Rojo, E, Titarenko, E, Sánchez-Serrano, JJ 1998Jasmonic acid-dependent and independent wound signal transduction pathways are differentially regulated by Ca2+/calmodulin in Arabidopsis thalianaMol Gen Genet258412419PubMedGoogle Scholar
  47. León, J, Rojo, E, Sánchez-Serrano, JJ 2001Wound signaling in plantsJ Exp Bot5219CrossRefGoogle Scholar
  48. Li, L, Li, C, Howe, GA 2001Genetic analysis of wound signaling in tomato. Evidence for a dual role of jasmonic acid in defense and female fertilityPlant Physiol12714141417PubMedGoogle Scholar
  49. Li, L, Li, C, Lee, GI, Howe, GA 2002aDistinct roles for jasmonic acid synthesis and action in the systemic wound response of tomatoProc Natl Acad Sci USA9964166421Google Scholar
  50. Li, C, Williams, MM, Loh, Y-T, Lee, GI, Howe, GA 2002bResistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathwayPlant Physiol130494503Google Scholar
  51. Li, C, Liu, G, Xu, C, Lee, GI, Bauer, P, Ling, HQ, Ganal, MW, Howe, GA 2003The tomato Suppressor of prosystemin-mediated responses2 (Spr2) gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signalPlant Cell1516461661PubMedGoogle Scholar
  52. Li, L, Zhao, Y, McCaig, BC, Wingerd, BA, Wang, J, Whalon, ME, Pichersky, E, Howe, GA 2004The tomato homolog of COI1 is required for maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome developmentPlant Cell16126143PubMedGoogle Scholar
  53. Lightner, J, Pearce, G, Ryan, CA, Browse, J 1993Isolation of signaling mutants of tomato (Lycopersicon esculentum)Mol Gen Genet241595601PubMedGoogle Scholar
  54. Maldonado, AM, Doerner, P, Dixon, RA, Lamb, CJ, Cameron, RK 2002A putative lipid transfer protein involved in systemic resistance signalling in ArabidopsisNature419399403CrossRefPubMedGoogle Scholar
  55. Malone, M 1996Rapid, long-distance signal transmission in higher plantsAdv Bot Res22163228Google Scholar
  56. Martin, DM, Gershenzon, J, Bohlmann, J 2003Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway sprucePlant Physiol13215861599CrossRefPubMedGoogle Scholar
  57. McConn, M, Creelman, RA, Bell, E, Mullet, JE, Browse, J 1997Jasmonate is essential for insect defense in ArabidopsisProc Natl Acad Sci USA.945473–5477Google Scholar
  58. McGurl, B, Pearce, G, Orozco-Cárdenas, M, Ryan, CA 1992Structure, expression, and antisense inhibition of the systemin precursor geneScience25515701573PubMedGoogle Scholar
  59. McGurl, B, Orozco-Cárdenas, M, Pearce, G, Ryan, CA 1994Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesisProc Natl Acad Sci USA9197999802PubMedGoogle Scholar
  60. Miersch, O, Wasternack, C 2000Octadecanoid and jasmonate signaling in tomato (Lycopersicon esculentum Mill.) leaves: endogenous jasmonates do not induce jasmonate biosynthesisBiol Chem381715722PubMedGoogle Scholar
  61. Narváez-Vásquez, J, Ryan, CA 2002The systemin precursor gene regulates both defensive and developmental genes in Solanum tuberosumProc Natl Acad Sci USA991581815821PubMedGoogle Scholar
  62. Narváez-Vásquez, J, Ryan, CA 2004The cellular localization of prosystemin: a functional role for phloem parenchyma in systemic wound signalingPlanta218360369PubMedGoogle Scholar
  63. Navazio, L, Moscatiello, R, Bellincampi, D, Baldan, B, Meggio, F, Brini, M, Bowler, C, Mariani, P 2002The role of calcium in oligogalacturonide-activated signalling in soybean cellsPlanta215596605PubMedGoogle Scholar
  64. Nishiuchi, T, Hamada, T, Kodoma, H, Iba, K 1997Wounding changes the spatial expression pattern of the Arabidopsis plastid ω3 fatty acid desaturase gene (FAD7) through different signal transduction pathwaysPlant Cell917011712PubMedGoogle Scholar
  65. O’Donnell, PJ, Calvert, C, Atzorn, R, Wasternack, C, Leyser, HMO, Bowles, DJ 1996Ethylene as a signal mediating the wound response of tomato plantsScience27419141917CrossRefPubMedGoogle Scholar
  66. O’Donnell, PJ, Truesdale, MR, Calvert, CM, Dorans, A, Roberts, MR, Bowles, DJ 1998A novel tomato gene that rapidly responds to wound- and pathogen-related signalsPlant J14137142PubMedGoogle Scholar
  67. Orians, CM, Pomerleau, J, Ricco, R 2000Vascular architecture generates fine scale variation in the systemic induction of proteinase inhibitors in tomatoJ Chem Ecol26471485Google Scholar
  68. Orozco-Cárdenas, M, McGurl, B, Ryan, CA 1993Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larvaeProc Natl Acad Sci USA9082738276PubMedGoogle Scholar
  69. Orozco-Cárdenas, M, Narvaez-Vasquez, J, Ryan, CA 2001Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonatePlant Cell13179191CrossRefPubMedGoogle Scholar
  70. Pautot, V, Holzer, FM, Walling, LL 1991Differential expression of tomato proteinase inhibitor I and II genes during bacterial pathogen invasion and woundingMol Plant-Microbe Interact4284292PubMedGoogle Scholar
  71. Peña-Cortés, H, Prat, S, Atzorn, R, Wasternack, C, Willmitzer, L 1996Abscisic acid-deficient plants do not accumulate proteinase inhibitor II following systemin treatmentPlanta198447451Google Scholar
  72. Rakwal, R, Agrawal, GK 2003Wound signaling-coordination of the octadecanoid and MAPK pathwaysPlant Physiol Biochem41855861Google Scholar
  73. Reymond, P, Weber, H, Damond, M, Farmer, EE 2000Differential gene expression in response to mechanical wounding and insect feeding in ArabidopsisPlant Cell12707720CrossRefPubMedGoogle Scholar
  74. Rojo, E, León, J, Sánchez-Serrano, JJ 1999aCross-talk between wound signaling pathways determines local versus systemic gene expression in Arabidopsis thalianaPlant J20135142Google Scholar
  75. Royo, J, Leon, J, Vancanneyt, G, Albar, JP, Rosahl, S, Ortego, F, Castanera, P, Sanchez-Serrano, JJ 1999bAntisense-mediated depletion of a potato lipoxygenase reduces wound induction of proteinase inhibitors and increases weight gain of insect pestsProc Natl Acad Sci USA9611461151Google Scholar
  76. Rojo, E, Solano, R, Sánchez-Serrano, JJ 2003Interactions between signaling compounds involved in plant defenseJ Plant Growth Regul228298Google Scholar
  77. Ryan, CA 1992The search for the proteinase inhibitor-inducing factor, PIIFPlant Mol Biol19123133PubMedGoogle Scholar
  78. Ryan, CA 2000The systemin signaling pathway: differential activation of plant defensive genesBiochim Biophys Acta1477112121CrossRefPubMedGoogle Scholar
  79. Ryan, CA, Moura, DS 2002Systemic wound signaling in plants: a new perceptionProc Natl Acad Sci USA9965196520PubMedGoogle Scholar
  80. Ryan, CA, Pearce, G 2003Systemins: a functionally defined family of peptide signals that regulate defensive genes in Solanaceae speciesProc Natl Acad Sci USA1001457714580PubMedGoogle Scholar
  81. Sagi, M, Davydov, O, Orazova, S, Yesbergenova, Z, Ophir, R, Stratmann, JW, Fluhr, R 2004Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentumPlant Cell16616628PubMedGoogle Scholar
  82. Sasaki, K, Hiraga, S, Ito, H, Seo, S, Matsui, H, Ohashi, Y 2002A wound-inducible tobacco peroxidase gene expresses preferentially in the vascular systemPlant Cell Physiol43108117PubMedGoogle Scholar
  83. Schafleitner, R, Wilhelm, E 2002Isolation of wound-responsive genes from chestmut (Catanea sativa) microstems by mRNA display and their differential expression upon wounding and infection with the chestnut blight fungus (Chryphonectria parasitica)Physiol Mol Plant Pathol61339348Google Scholar
  84. Scheer, JM, Ryan, CA 1999A 160-kD systemin receptor on the surface of Lycopersicon peruvianum suspension-cultured cellsPlant Cell1115251536CrossRefPubMedGoogle Scholar
  85. Scheer, JM, Ryan, CA 2002The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase familyProc Natl Acad Sci USA9995859590Google Scholar
  86. Schittko, U, Hermsmeier, D, Baldwin, IT 2001Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IIAccumulation of plant mRNAs in response to insect-derived cues. Plant Physiol125701710Google Scholar
  87. Schittko, U, Baldwin, IT 2003Constraints to herbivore-induced systemic responses: bidirectional signaling along orthostichies in Nicotiana attenuataJ Chem Ecol29763770PubMedGoogle Scholar
  88. Seo, S, Okamoto, M, Seto, H, Ishizuka, K, Sano, H, Ohashi, Y 1995Tobacco MAP kinase: a possible mediator in wound signal transduction pathwaysScience27019881992PubMedGoogle Scholar
  89. Seo, S, Sano, H, Ohashi, Y 1999Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinasePlant Cell11289298PubMedGoogle Scholar
  90. Seo, HS, Song, JT, Cheong, JJ, Lee, YH, Lee, YW, Hwang, I, Lee, JS, Choi, YD 2001Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responsesProc Natl Acad Sci USA9847884793PubMedGoogle Scholar
  91. Staswick, PE, Tiryaki, I 2004The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine ArabidopsisPlant Cell1621172127PubMedGoogle Scholar
  92. Staswick, PE, Tiryaki, I, Rowe, ML 2002Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylationPlant Cell1414051415CrossRefPubMedGoogle Scholar
  93. Stenzel, I, Hause, B, Maucher, H, Pitzschke, A, Miersch, O, Ziegler, J, Ryan, CA, Wasternack, C 2003Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato—amplification in wound signallingPlant J33577589PubMedGoogle Scholar
  94. Strassner, J, Schaller, F, Frick, U, Howe, GA, Weiler, EW, Amrhein, N, Macheroux, P, Schaller, A 2002Characterization and cDNA-microarray expression analysis of 12-oxophytodienoate reductases reveals differential roles for octadecanoid biosynthesis in the local versus the systemic wound responsePlant J32585601CrossRefPubMedGoogle Scholar
  95. Stratmann, J 2003Long distance run in the wound response—jasmonic acid pulls aheadTrends Plant Sci8247250PubMedGoogle Scholar
  96. Stratmann, JW, Ryan, CA 1997Myelin basic protein kinase activity in tomato leaves is induced systemically by wounding and increases in response to systemin and oligosaccharide elicitorsProc Natl Acad Sci USA941108511089PubMedGoogle Scholar
  97. Stuhlfelder, C, Mueller, MJ, Warzecha, H 2004Cloning and expression of a tomato cDNA encoding a methyl jasmonate cleaving esteraseEur J Biochem27129762983PubMedGoogle Scholar
  98. Swiatek, A, Dongen, W, Esmans, EL, Onckelen, H 2004Metabolic fate of jasmonates in tobacco bright yellow-2 cellsPlant Physiol135161172PubMedGoogle Scholar
  99. Thaler, JS, Farag, MA, Paré, PW, Dicke, M 2002Jasmonate-deficient plants have reduced direct and indirect defences against herbivoresEcol Lett5764774Google Scholar
  100. Thaler, JS, Owen, B, Higgins, VJ 2004The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestylesPlant Physiol135530538PubMedGoogle Scholar
  101. Titarenko, E, Rojo, E, León, J, Sánchez-Serrano, JJ 1997Jasmonic acid-dependent and independent signaling pathways control wound-induced gene activation in Arabidopsis thalianaPlant Physiol11817826Google Scholar
  102. Truitt, CL, Pare, PW 2004In situ translocation of volicitin by beet armyworm larvae to maize and systemic immobility of the herbivore elicitor inplantaPlanta2189991007PubMedGoogle Scholar
  103. Truitt, CL, Wei, HX, Paré, PW 2004A plasma membrane protein from Zea mays binds with the herbivore elicitor volicitinPlant Cell16523532PubMedGoogle Scholar
  104. Turner, JG, Ellis, C, Devoto, A 2002The jasmonate signal pathwayPlant Cell. S153S164Google Scholar
  105. Van der Hoeven, R, Ronning, C, Giovannoni, J, Martin, G, Tanksley, S 2002Deductions about the number, organization, and evolution of genes in the tomato genome based on analysis of a large expressed sequence tag collection and selective genomic sequencingPlant Cell1414411456PubMedGoogle Scholar
  106. Vijayan, P, Shockey, J, Levesque, CA, Cook, RJ, Browse, J 1998A role for jasmonate in pathogen defense of ArabidopsisProc Natl Acad Sci USA9572097214CrossRefPubMedGoogle Scholar
  107. von Dahl, CC, Baldwin, IT 2004Methyl jasmonate and cis-jasmone do not dispose of the herbivore-induced jasmonate burst in Nicotiana attenuataPhysiol Plant120474481PubMedGoogle Scholar
  108. Vorwerk, S, Somerville, S, Somerville, C 2004The role of plant cell wall polysaccharide composition in disease resistanceTrends Plant Sci9203209PubMedGoogle Scholar
  109. Walling, LL 2000The myriad plant responses to herbivoresJ Plant Growth Regul19195216PubMedGoogle Scholar
  110. Walz, C, Giavalisco, P, Schad, M, Juenger, M, Klose, J, Kehr, J 2004Proteomics of curcurbit phloem exudate reveals a network of defence proteinsPhytochemistry6517951804Google Scholar
  111. Wang, C, Zien, CA, Afitlhile, M, Welti, R, Hildebrand, DF, Wang, X 2000Involvement of phospholipase D in wound-induced accumulation of jasmonic acid in ArabidopsisPlant Cell1222372246Google Scholar
  112. Wang, ZY, He, JX 2004Brassinosteroid signal transduction—choices of signals and receptorsTrends Plant Sci99196PubMedGoogle Scholar
  113. Wasternack, C, Hause, B 2002Jasmonates and octadecanoids: signals in plant stress responses and developmentProg Nucleic Acid Res Mol Biol72165221Google Scholar
  114. Weber, H 2002Fatty acid-derived signals in plantsTrends Plant Sci7217224PubMedGoogle Scholar
  115. Wendehenne, D, Durner, J, Klessig, DF 2004Nitric oxide: a new player in plant signaling and defenceCurr Opin Plant Biol7449455PubMedGoogle Scholar
  116. Xie, DX, Feys, BF, James, S, Nieto-Rostro, M, Turner, JG 1998COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertilityScience28010911094CrossRefPubMedGoogle Scholar
  117. Xu, LH, Liu, FQ, Lechner, E, Genschik, P, Crosby, WL, Ma, H, Peng, W, Huang, DF, Xie, DX 2002The SCFCOI1 ubiquitin-ligase complexes are required for jasmonate response in ArabidopsisPlant Cell1419191935PubMedGoogle Scholar
  118. Yamada, K, Nishimura, M, Hara-Nishimura, I 2004The slow wound-response of γVPE is regulated by endogenous salicylic acid in ArdbidopsisPlanta218599605PubMedGoogle Scholar
  119. Zhang, Z-P, Baldwin, IT 1997Transport of [2–14C] jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris.Planta203436441Google Scholar
  120. Zhao, Y, Thilmony, R, Bender, C, He, SY, Howe, GA 2003The Hrp type III secretion system and coronatine of Pseudomonas syringae pv. tomato coordinately modify host defense by targeting the jasmonate signaling pathway in tomatoPlant J36485499PubMedGoogle Scholar
  121. Ziegler, J, Keinänen, M, Baldwin, IT 2001Herbivore-induced allene oxide synthase transcripts and jasmonic acid in Nicotiana attenuataPhytochemistry58729738PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2004

Authors and Affiliations

  1. 1.Department of Energy Plant Research Laboratory, and Department of Biochemistry and Molecular BiologyMichigan State UniversityEast LansingUSA

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