Advertisement

Plant Molecular Biology

, Volume 58, Issue 4, pp 497–513 | Cite as

Expression profiling reveals COI1 to be a key regulator of genes involved in wound- and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions

  • Alessandra Devoto
  • Christine Ellis
  • Andreas Magusin
  • Hur-Song Chang
  • Charles Chilcott
  • Tong Zhu
  • John G. Turner
Article

Abstract

The Arabidopsis gene COI1 is required for jasmonic acid (JA)-induced growth inhibition, resistance to insect herbivory, and resistance to pathogens. In addition, COI1 is also required for transcription of several genes induced by wounding or by JA. Here, we use microarray gene transcription profiling of wild type and coi1 mutant plants to examine the extent of the requirement of COI1 for JA-induced and wound-induced gene transcription. We show that COI1 is required for expression of approximately 84% of 212 genes induced by JA, and for expression of approximately 44% of 153 genes induced by wounding. Surprisingly, COI1 was also required for repression of 53% of 104 genes whose expression was suppressed by JA, and for repression of approximately 46% of 83 genes whose expression was suppressed by wounding. These results indicate that COI1 plays a pivotal role in wound- and JA signalling.

Keywords

Jasmonate, Microarray, COI1 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

Fig S1.pdf (5.9 mb)
Fig S1 (PDF 6.045 KB)
Fig S2.pdf (7.3 mb)
Fig S2 (PDF 7.428 KB)
Fig S3.pdf (6.3 mb)
Fig S3 (PDF 6.472 KB)
Fig S4.pdf (6.8 mb)
Fig S4 (PDF 6.944 KB)
Fig S5.pdf (2.1 mb)
Fig S5 (PDF 2.145 KB)
Fig S6.pdf (1.2 mb)
Fig S6 (PDF 1.249 KB)
Table SI.xls (312 kb)
Table SI (XLS 312 KB)
Table SII.xls (198 kb)
Table SII (XLS 199 KB)
Table SIII.xls (72 kb)
Table SIII (XLS 72 KB)

References

  1. Anderson, J.P., Badruzsaufari, E., Schenk, P.M., Manners, J.M., Desmond, O.J., Ehlert, C., Maclean, D.J., Ebert, P.R., Kazan, K. 2004Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in ArabidopsisPlant Cell1634603479PubMedCrossRefGoogle Scholar
  2. Armengaud, P., Breitling, R., Amtmann, A. 2004The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signalingPlant Physiol.13625562576PubMedCrossRefGoogle Scholar
  3. Aubourg, S., Lecharny, A., Bohlmann, J. 2002Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana Mol. Genet. Genomics267730745PubMedCrossRefGoogle Scholar
  4. Bell, E., Mullet, J.E. 1993Characterization of an Arabidopsis lipoxygenase gene responsive to methyl jasmonate and woundingPlant Physiol.10311331137PubMedCrossRefGoogle Scholar
  5. Bender, J., Fink, G.R. 1998A Myb homologue, ATR1, activates tryptophan gene expression in Arabidopsis Proc. Natl. Acad. Sci. USA9556555660PubMedCrossRefGoogle Scholar
  6. Benedetti, C.E., Xie, D., Turner, J.G. 1995Coi1-dependent expression of an Arabidopsis vegetative storage protein in flowers and siliques and in response to coronatine or methyl jasmonatePlant Physiol.109567572PubMedCrossRefGoogle Scholar
  7. Benedetti, C.E., Arruda, P. 2002Altering the expression of the chlorophyllase gene ATHCOR1 in transgenic Arabidopsis caused changes in the chlorophyll-to-chlorophyllide ratioPlant Physiol.12812551263PubMedCrossRefGoogle Scholar
  8. Benjamini, Y., Hochberg, Y. 1995Controlling the false discovery rate: a practical and powerful approach to multiple testingJ. Roy. Stat. Soc. B57289300Google Scholar
  9. Birkett, M.A., Campbell, C.A., Chamberlain, K., Guerrieri, E., Hick, A.J., Martin, J.L., Matthes, M., Napier, J.A., Pettersson, J., Pickett, J.A., Poppy, G.M., Pow, E.M., Pye, B.J., Smart, L.E., Wadhams, G.H., Wadhams, L.J., Woodcock, C.M. 2000New roles for cis-jasmone as an insect semiochemical and in plant defenseProc. Natl. Acad. Sci. USA9793299334PubMedCrossRefGoogle Scholar
  10. Bohlmann, H., Vignutelli, A., Hilpert, B., Miersch, O., Wasternack, C., Apel, K. 1998Wounding and chemicals induce expression of the Arabidopsis thaliana gene Thi2.1, encoding a fungal defense thionin, via the octadecanoid pathwayFEBS Lett.437281286PubMedCrossRefGoogle Scholar
  11. Borevitz, J.O., Xia, Y., Blount, J., Dixon, R.A., Lamb, C. 2000Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesisPlant Cell1223832394PubMedCrossRefGoogle Scholar
  12. Brader, G., Tas, E., Palva, E.T. 2001Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora Plant Physiol.126849860PubMedCrossRefGoogle Scholar
  13. Capella, A.N., Menossi, M., Arruda, P., Benedetti, C.E. 2001COI1 affects myrosinase activity and controls the expression of two flower-specific myrosinase-binding protein homologues in Arabidopsis Planta213691699PubMedCrossRefGoogle Scholar
  14. Chen, W., Provart, N.J., Glazebrook, J., Katagiri, F., Chang, H.S., Eulgem, T., Mauch, F., Luan, S., Zou, G., Whitham, S.A., Budworth, P.R., Tao, Y., Xie, Z., Chen, X., Lam, S., Kreps, J.A., Harper, J.F., Si-Ammour, A., Mauch-Mani, B., Heinlein, M., Kobayashi, K., Hohn, T., Dangl, J.L., Wang, X., Zhu, T. 2002Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stressesPlant Cell14559574PubMedCrossRefGoogle Scholar
  15. Chen, F., Tholl, D., D’Auria, J.C., Farooq, A., Pichersky, E., Gershenzon, J. 2003Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowersPlant Cell15481494PubMedCrossRefGoogle Scholar
  16. Cheong, Y.H., Chang, H.S., Gupta, R., Wang, X., Zhu, T., Luan, S. 2002Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis Plant Physiol.129 661677PubMedCrossRefGoogle Scholar
  17. Creelman, R.A., Tierney, M.L., Mullet, J.E. 1992Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expressionProc. Natl. Acad. Sci. USA8949384941PubMedCrossRefGoogle Scholar
  18. Devoto, A., Nieto-Rostro, M., Xie, D., Ellis, C., Harmston, R., Patrick, E., Davis, J., Sherratt, L., Coleman, M., Turner, J.G. 2002COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis Plant J.32457466PubMedCrossRefGoogle Scholar
  19. Devoto, A., Turner, J.G. 2003Regulation of jasmonate-mediated plant responses in Arabidopsis Ann. Bot. (Lond)92329337CrossRefGoogle Scholar
  20. Devoto, A., Turner, J.G. 2005Jasmonate-regulated Arabidopsis stress signalling networkPhys. Plant123161172CrossRefGoogle Scholar
  21. Eisen, M.B., Spellman, P.T., Brown, P.O., Botstein, D. 1998Cluster analysis and display of genome-wide expression patternsProc. Natl. Acad. Sci. USA951486314868PubMedCrossRefGoogle Scholar
  22. Ellis, C., Turner, J.G. 2001The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogensPlant Cell1310251033PubMedCrossRefGoogle Scholar
  23. Ellis, C., Turner, J.G. 2002A conditionally fertile coi1 allele indicates cross-talk between plant hormone signalling pathways in Arabidopsis thaliana seeds and young seedlingsPlanta215549556PubMedCrossRefGoogle Scholar
  24. Ellis, C., Karafyllidis, I., Turner, J.G. 2002Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae Mol. Plant–Microbe. Interact.1510251030PubMedGoogle Scholar
  25. Fabbri, M., Delp, G., Schmidt, O., Theopold, U. 2000Animal and plant members of a gene family with similarity to alkaloid-synthesizing enzymesBiochem. Biophys. Res. Commun.271191196PubMedCrossRefGoogle Scholar
  26. Facchini, P.J., Bird, D.A., St-Pierre, B. 2004Can Arabidopsis make complex alkaloids?Trend. Plant Sci.9116122CrossRefGoogle Scholar
  27. Faldt, J., Arimura, G., Gershenzon, J., Takabayashi, J., Bohlmann, J. 2003Functional identification of AtTPS03 as (E)-beta-ocimene synthase: a monoterpene synthase catalyzing jasmonate- and wound-induced volatile formation in Arabidopsis thaliana Planta216745751PubMedGoogle Scholar
  28. Farmer, E.E., Ryan, C.A. 1990Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leavesProc. Natl. Acad. Sci. USA8777137716PubMedCrossRefGoogle Scholar
  29. Feng, S., Ma, L., Wang, X., Xie, D., Dinesh-Kumar, S.P., Wei, N., Deng, X.W. 2003The COP9 signalosome interacts physically with SCF COI1 and modulates jasmonate responsesPlant Cell1510831094PubMedCrossRefGoogle Scholar
  30. Feys, B., Benedetti, C.E., Penfold, C.N., Turner, J.G. 1994 Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogenPlant Cell6751759PubMedCrossRefGoogle Scholar
  31. Feys, B.J., Parker, J.E. 2000Interplay of signaling pathways in plant disease resistanceTrend. Genet.16449455CrossRefGoogle Scholar
  32. Genoud, T., Trevino Santa Cruz, M.B., Metraux, J.P. 2001Numeric simulation of plant signaling networksPlant Physiol.12614301437PubMedCrossRefGoogle Scholar
  33. Glazebrook, J., Chen, W., Estes, B., Chang, H.S., Nawrath, C., Metraux, J.P., Zhu, T., Katagiri, F. 2003Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotypingPlant J.34217228PubMedCrossRefGoogle Scholar
  34. Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., Hornik, K., Hothorn, T., Huber, W., Iacus, S., Irizarry, R., Leisch, F., Li, C., Maechler, M., Rossini, A.J., Sawitzki, G., Smith, C., Smyth, G., Tierney, L., Yang, J.Y.H., Zhang, J. 2004Bioconductor: Open software development for computational biology and bioinformaticsGenome. Biol.5R80PubMedCrossRefGoogle Scholar
  35. Glonek, G.F.V., Solomon, P.J. 2004Factorial and time course designs for cDNA microarray experimentsBiostatistics589111PubMedCrossRefGoogle Scholar
  36. Gundlach, H., Muller, M.J., Kutchan, T.M., Zenk, M.H. 1992Jasmonic acid is a signal transducer in elicitor-induced plant cell culturesProc. Natl. Acad. Sci. USA8923892393PubMedCrossRefGoogle Scholar
  37. Harmer, S.L., Hogenesch, J.B., Straume, M., Chang, H.S., Han, B., Zhu, T., Wang, X., Kreps, J.A., Kay, S.A. 2000Orchestrated transcription of key pathways in Arabidopsis by the circadian clockScience29021102113PubMedCrossRefGoogle Scholar
  38. Kang, J.Y., Choi, H.I., Im, M.Y., Kim, S.Y. 2002 Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signalingPlant Cell14 343357PubMedCrossRefGoogle Scholar
  39. Kloek, A.P., Verbsky, M.L., Sharma, S.B., Schoelz, J.E., Vogel, J., Klessig, D.F., Kunkel, B.N. 2001Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanismsPlant J.26509522PubMedCrossRefGoogle Scholar
  40. Kranz, H.D., Denekamp, M., Greco, R., Jin, H., Leyva, A., Meissner, R.C., Petroni, K., Urzainqui, A., Bevan, M., Martin, C., Smeekens, S., Tonelli, C., Paz-Ares, J., Weisshaar, B. 1998Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana Plant J.16263276PubMedCrossRefGoogle Scholar
  41. Ihaka, R., Gentleman, R. 1996R: A language for data analysis and graphicsJ. Comput. Graph. Stat.5299314CrossRefGoogle Scholar
  42. Laudert, D., Weiler, E.W. 1998Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signallingPlant J.15675684PubMedCrossRefGoogle Scholar
  43. Lee, Y.H., Chun, J.Y. 1998A new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatmentPlant Mol. Biol.37377384PubMedCrossRefGoogle Scholar
  44. Li, J., Brader, G., Palva, E.T. 2004The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defensePlant Cell16319331PubMedCrossRefGoogle Scholar
  45. Liscum, E., Reed, J.W. 2002Genetics of Aux/IAA and ARF action in plant growth and developmentPlant Mol. Biol.49387400PubMedCrossRefGoogle Scholar
  46. Lorenzo, O., Piqueras, R., Sanchez-Serrano, J.J., Solano, R. 2003ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defensePlant Cell15165178PubMedCrossRefGoogle Scholar
  47. Lorenzo, O., Chico, J.M., Sanchez-Serrano, J.J., Solano, R. 2004Jasmonate-insensitive1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defence responses in Arabidopsis Plant Cell16193850PubMedCrossRefGoogle Scholar
  48. Mandaokar, A., Dinesh Kumar, V., Amway, M., Browse, J. 2003Microarray and differential display identify genes involved in jasmonate-dependent anther developmentPlant Mol. Biol.52775786PubMedCrossRefGoogle Scholar
  49. McConn, M., Browse, J. 1996The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis MutantPlant Cell8403416PubMedCrossRefGoogle Scholar
  50. McConn, M., Creelman, R.A., Bell, E., Mullet, J.E., Browse, J. 1997Jasmonate is essential for insect defense in Arabidopsis Proc. Natl. Acad. Sci. USA9454735477PubMedCrossRefGoogle Scholar
  51. Menke, F.L., Champion, A., Kijne, J.W., Memelink, J. 1999A novel jasmonate- and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate- and elicitor-inducible AP2-domain transcription factor, ORCA2Embo. J.1844554463PubMedCrossRefGoogle Scholar
  52. Mikkelsen, M.D., Hansen, C.H., Wittstock, U., Halkier, B.A. 2000Cytochrome P450 CYP79B2 from Arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acidJ.␣Biol. Chem.2753371233717PubMedCrossRefGoogle Scholar
  53. Nagpal, P., Walker, L.M., Young, J.C., Sonawala, A., Timpte, C., Estelle, M., Reed, J.W. 2000AXR2 encodes a member␣of␣the Aux/IAA protein familyPlant Physiol.123563574PubMedCrossRefGoogle Scholar
  54. Orozco-Cardenas, M., Narvaez-Vasquez, J., Ryan, C. 2001Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonatePlant Cell13179191PubMedCrossRefGoogle Scholar
  55. Overmyer, K., Tuominen, H., Kettunen, R., Betz, C., Langebartels, C., Sandermann, H., Kangasjarvi, J. 2000Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell deathPlant Cell1218491862PubMedCrossRefGoogle Scholar
  56. Penninckx, I.A., Thomma, B.P., Buchala, A., Metraux, J.P., Broekaert, W.F. 1998Concomitant activation of jasmonate and ethylene response pathways is required for induction of␣a plant defensin gene in Arabidopsis Plant Cell10 21032113PubMedCrossRefGoogle Scholar
  57. Pieterse, C.M., Wees, S.C., Pelt, J.A., Knoester, M., Laan, R., Gerrits, H., Weisbeek, P.J., Loon, L.C. 1998A novel signaling pathway controlling induced systemic resistance in Arabidopsis Plant Cell1015711580PubMedCrossRefGoogle Scholar
  58. Puthoff, D.P., Nettleton, D., Rodermel, S.R., Baum, T.J. 2003 Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profilesPlant J.33911921PubMedCrossRefGoogle Scholar
  59. Quattrocchio, F., Wing, J.F., Woude, K., Mol, J.N., Koes, R. 1998Analysis of bHLH and MYB domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genesPlant J.13475488PubMedCrossRefGoogle Scholar
  60. Rao, M.V., Lee, H., Creelman, R.A., Mullet, J.E., Davis, K.R. 2000Jasmonic acid signaling modulates ozone-induced hypersensitive cell deathPlant Cell1216331646PubMedCrossRefGoogle Scholar
  61. Rask, L., Andreasson, E., Ekbom, B., Eriksson, S., Pontoppidan, B., Meijer, J. 2000Myrosinase: gene family evolution and herbivore defense in BrassicaceaePlant Mol. Biol.4293113PubMedCrossRefGoogle Scholar
  62. Reymond, P., Weber, H., Damond, M., Farmer, E.E. 2000Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis Plant Cell12707720PubMedCrossRefGoogle Scholar
  63. Reymond, P., Bodenhausen, N., Poecke, R.M., Krishnamurthy, V., Dicke, M., Farmer, E.E. 2004A conserved transcript pattern in response to a specialist and a generalist herbivorePlant Cell1631323147PubMedCrossRefGoogle Scholar
  64. Roberts, S.C., Shuler, M.L. 1997Large-scale plant cell cultureCurr. Opin. Biotechnol.8154159PubMedCrossRefGoogle Scholar
  65. Rojo, E., Titarenko, E., Leon, J., Berger, S., Vancanneyt, G., Sanchez-Serrano, J.J. 1998Reversible protein phosphorylation regulates jasmonic acid-dependent and -independent wound signal transduction pathways in Arabidopsis thaliana Plant J.13153165PubMedCrossRefGoogle Scholar
  66. Rojo, E., Leon, J., Sanchez-Serrano, J.J. 1999Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana Plant J.20135142PubMedCrossRefGoogle Scholar
  67. Sanders, P.M., Lee, P.Y., Biesgen, C., Boone, J.D., Beals, T.P., Weiler, E.W., Goldberg, R.B. 2000The Arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathwayPlant Cell1210411061PubMedCrossRefGoogle Scholar
  68. Sandorf, I., Holländer-Czytko, H. 2002Jasmonate is involved in the induction of tyrosine aminotransferase and tocopherol biosynthesis in Arabidopsis thaliana Planta216173179PubMedCrossRefGoogle Scholar
  69. Sasaki, Y., Asamizu, E., Shibata, D., Nakamura, Y., Kaneko, T., Awai, K., Amagai, M., Kuwata, C., Tsugane, T., Masuda, T., Shimada, H., Takamiya, K., Ohta, H., Tabata, S. 2001Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathwaysDNA Res.8153161PubMedCrossRefGoogle Scholar
  70. Schenk, P.M., Kazan, K., Wilson, I., Anderson, J.P., Richmond, T., Somerville, S.C., Manners, JM 2000Coordinated plant defense responses in Arabidopsis revealed by microarray analysisProc. Natl. Acad. Sci. USA971165511660PubMedCrossRefGoogle Scholar
  71. Schmeller, T.T., Latz-Bruning, B., Wink, M. 1997Biochemical activities of berberine, palmatine and sanguinarine mediating chemical defence against microorganisms and herbivoresPhytochemistry44257266PubMedCrossRefGoogle Scholar
  72. Searle, S.R. 1971 Linear ModelsWileyNew YorkGoogle Scholar
  73. Smyth, G.K. 2004Linear models and empirical Bayes methods for assessing differential expression in microarray experimentsStat. Appl. Genet. Mol. Biol.3125Google Scholar
  74. Staswick, P.E., Yuen, G.Y., Lehman, C.C. 1998Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregularePlant J.15747754PubMedCrossRefGoogle Scholar
  75. Staswick, P.E., Tiryaki, I., Rowe, M.L. 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 Cell1414051415PubMedCrossRefGoogle Scholar
  76. Stintzi, A., Browse, J. 2000The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesisProc. Natl. Acad. Sci. USA971062510630PubMedCrossRefGoogle Scholar
  77. Suzuki, H., Achnine, L., Xu, R., Matsuda, S.P.T., Dixon, R.A. 2002A genomics approach to the early stages of triterpene saponin biosynthesis in Medicago truncatula Plant J.3210331048PubMedCrossRefGoogle Scholar
  78. Thomma, B.P., Eggermont, K., Penninckx, I., Mauch-Mani, B., Vogelsang, R., Cammue, B.P.A., Broekaert, W.F. 1998Separate jasmonate-dependent and salicylate-dependent defense–response pathways in Arabidopsis are essential for resistance to distinct microbial pathogensProc. Natl. Acad. Sci. USA951510715111CrossRefPubMedGoogle Scholar
  79. Thomma, B.P., Nelissen, I., Eggermont, K., Broekaert, W.F. 1999Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola Plant J. 199919163171Google Scholar
  80. Titarenko, E., Rojo, E., Leon, J., Sanchez-Serrano, J.J. 1997Jasmonic acid-dependent and -independent signaling pathways control wound-induced gene activation in Arabidopsis thaliana Plant Physiol.115817826PubMedCrossRefGoogle Scholar
  81. Tsuji, J., Jackson, E.P., Gage, D.A., Hammerschmidt, R., Somerville, S.C. 1992Phytoalexin accumulation in Arabidopsis thaliana during the hypersensitive reaction to Pseudomonas syringae pv syringaePlant Physiol.9813041309PubMedCrossRefGoogle Scholar
  82. Turner, J.G., Ellis, C., Devoto, A. 2002The jasmonate signal pathwayPlant Cell14S153S164PubMedGoogle Scholar
  83. Fits, L., Memelink, J. 2000ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolismScience289295297PubMedCrossRefGoogle Scholar
  84. Poecke, R.M., Posthumus, M.A., Dicke, M. 2001Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysisJ. Chem. Ecol.27191128PubMedCrossRefGoogle Scholar
  85. Weiler, E.W., Kutchan, T.M., Gorba, T., Brodschelm, W., Niesel, U., Bublitz, F. 1994The Pseudomonas phytotoxin coronatine mimics octadecanoid signalling molecules of higher plantsFEBS Lett.345913PubMedCrossRefGoogle Scholar
  86. Wernisch, L., Kendall, S.L., Soneji, S., Wietzorrek, A., Parish, T., Hinds, J., Butcher, P.D., Stoker, N.G. 2003Analysis of whole-genome microarray replicates using mixed modelsBioinformatics195361PubMedCrossRefGoogle Scholar
  87. Wittstock, U., Halkier, B.A. 2002Glucosinolate research in the Arabidopsis eraTrend. Plant Sci.7263270CrossRefGoogle Scholar
  88. Wu, Z., Irizarry, R.A., Gentleman, R., Martinez-Murillo, F., Spencer, F. 2004A model-based background adjustment for oligonucleotide expression arraysJ. Am. Stat. Assoc.99909917CrossRefGoogle Scholar
  89. Xie, D.X., Feys, B.F., James, S., Nieto-Rostro, M., Turner, J.G. 1998COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertilityScience28010911094PubMedCrossRefGoogle Scholar
  90. Xu, Y., Chang, P., Liu, D., Narasimhan, M.L., Raghothama, K.G., Hasegawa, P.M., Bressan, R.A. 1994Plant defense genes are synergistically induced by ethylene and methyl jasmonatePlant Cell610771085PubMedCrossRefGoogle Scholar
  91. Xu, L., Liu, F., Lechner, E., Genschik, P., Crosby, W.L., Ma, H., Peng, W., Huang, D., Xie, D. 2002The SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis Plant Cell1419191935PubMedCrossRefGoogle Scholar
  92. Zhao, Y., Hull, A.K., Gupta, N.R., Goss, K.A., Alonso, J., Ecker, J.R., Normanly, J., Chory, J., Celenza, J.L. 2002Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3Genes Dev.1631003112PubMedCrossRefGoogle Scholar
  93. Zhu, T., Wang, X. 2000Large-scale profiling of the Arabidopsis transcriptomePlant Physiol.12414726PubMedCrossRefGoogle Scholar
  94. Zhu, T., Budworth, P., Han, B., Brown, D., Chang, H-S., Zou, G., Wang, X. 2001Toward elucidating the global gene expression patterns of developing Arabidopsis: Parallel analysis of 8300 genes by a high-density oligonucleotide probe arrayPlant Physiol. Biochem.39221242CrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Alessandra Devoto
    • 1
  • Christine Ellis
    • 1
    • 5
  • Andreas Magusin
    • 2
  • Hur-Song Chang
    • 3
    • 6
  • Charles Chilcott
    • 3
  • Tong Zhu
    • 3
    • 4
  • John G. Turner
    • 1
  1. 1.School of Biological SciencesUniversity of East AngliaNorwichUK
  2. 2.John Innes CentreNorwichUK
  3. 3.Torrey Mesa Research Institute, Syngenta Research and TechnologySan DiegoUSA
  4. 4.Syngenta Biotechnology Inc.Research Triangle ParkUSA
  5. 5.Department of BiologyUniversity of North Carolina at Chapel HillChapel HillUSA
  6. 6.Diversa CorporationSan DiegoUSA;

Personalised recommendations