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Planta

, Volume 232, Issue 5, pp 1163–1180 | Cite as

The transcriptome of cis-jasmone-induced resistance in Arabidopsis thaliana and its role in indirect defence

  • Michaela C. Matthes
  • Toby J. A. Bruce
  • Jurriaan Ton
  • Paul J. Verrier
  • John A. Pickett
  • Johnathan A. Napier
Original Article

Abstract

cis-jasmone (CJ) is a plant-derived chemical that enhances direct and indirect plant defence against herbivorous insects. To study the signalling pathway behind this defence response, we performed microarray-based transcriptome analysis of CJ-treated Arabidopsis plants. CJ influenced a different set of genes from the structurally related oxylipin methyl jasmonate (MeJA), suggesting that CJ triggers a distinct signalling pathway. CJ is postulated to be biosynthetically derived from jasmonic acid, which can boost its own production through transcriptional up-regulation of the octadecanoid biosynthesis genes LOX2,AOS and OPR3. However, no effect on these genes was detected by treatment with CJ. Furthermore, CJ-responsive genes were not affected by mutations in COI1 or JAR1, which are critical signalling components in MeJA response pathway. Conversely, a significant proportion of CJ-inducible genes required the three transcription factors TGA2, TGA5 and TGA6, as well as the GRAS regulatory protein SCARECROW-like 14 (SCL14), indicating regulation by a different pathway from the classical MeJA response. Moreover, the biological importance was demonstrated in that mutations in TGA2, 5, 6, SCL14 and the CJ-inducible gene CYP81D11 blocked CJ-induced attraction of the aphid parasitoid Aphidius ervi, demonstrating that these components play a key role in CJ-induced indirect defence. Collectively, our results identify CJ as a member of the jasmonates that controls indirect plant defence through a distinct signalling pathway.

Keywords

Indirect defence Jasmonate signalling cis-Jasmone Tritrophic interactions 

Abbreviations

CJ

cis-Jasmone

JA

Jasmonic acid

MeJA

Methyl jasmonate

MDA

Malondialdehyde

MVK

Methyl vinyl ketone

OPDA

12-Oxophytodienoic acid

PPA

Phytoprostanes

RES

Reactive electrophile species

Notes

Acknowledgments

Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council BBSRC (UK). The authors thank Christiane Gatz (University of Göttingen, Germany) for helpful discussions and the SCL14 lines. Research activities by Jurriaan Ton are supported by a BBSRC Institute Career Path Fellowship (BB/E023959/1).

Supplementary material

425_2010_1244_MOESM1_ESM.ppt (1.5 mb)
Supplementary material 1 (PPT 1.51 mb)
425_2010_1244_MOESM2_ESM.doc (104 kb)
Supplementary material 2 (DOC 103 kb)

References

  1. Alméras E, Stolz S, Vollenweider S, Reymond P, Mène-Saffrané L, Farmer EE (2003) Reactive electrophile species activate defense gene expression in Arabidopsis. Plant J 34:205–216CrossRefPubMedGoogle Scholar
  2. Baerson SR, Sanchez-Moreiras A, Pedrol-Bonjoch N, Schulz M, Kagan IA, Agarwal AK, Reigosa MJ, Duke SO (2005) Detoxification and transcriptome response in Arabidopsis seedlings exposed to the allelochemical benzoxazolin-2(3H)-one. J Biol Chem 280:21867–21881CrossRefPubMedGoogle Scholar
  3. Bate NS, Rothstein SJ (1998) C6-volatiles derived from the lipoxygenase pathway induce a subset of defence-related genes. Plant J 16:561–569CrossRefPubMedGoogle Scholar
  4. Birkett MA, Campbell CAM, Chamberlain K, Guerrieri E, Hick AJ, Martin JL, Matthes MC, Napier JA, Pettersson J, Pickett JA, Poppy GM, Pow EM, Pye BJ, Smart LE, Wadhams LJ, Wadhams GH, Woodcock CM (2000) New roles for cis-jasmone as an insect semiochemical and in plant defense. Proc Natl Acad Sci USA 97:9329–9334CrossRefPubMedGoogle Scholar
  5. Blee E (2002) Impact of phyto-oxylipins in plant defense. Trends Plant Sci 7:315–321CrossRefPubMedGoogle Scholar
  6. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on bias and variance. Bioinformatics 19:185–193CrossRefPubMedGoogle Scholar
  7. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Goerlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510CrossRefPubMedGoogle Scholar
  8. Bruce TJ, Pickett JA (2007) Plant defence signalling induced by biotic attacks. Curr Opin Plant Biol 10:387–392CrossRefPubMedGoogle Scholar
  9. Bruce TJA, Martin JL, Pickett JA, Pye BJ, Smart LE, Wadhams L (2003) cis-Jasmone treatment induces resistance in wheat plants against the grain aphid, Stibion avenae (Fabricius) (Homoptera:Aphididae). Pest Manag Sci 59:1031–1036CrossRefPubMedGoogle Scholar
  10. Bruce TJ, Matthes MC, Chamberlain K, Woodcock CM, Mohib A, Webster B, Smart LE, Birkett MA, Pickett JA, Napier JA (2008) cis-Jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and their parasitoids. Proc Natl Acad Sci USA 105:4553–4558CrossRefPubMedGoogle Scholar
  11. Chini A, Fonseca S, Fernandez GT, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671CrossRefPubMedGoogle Scholar
  12. Chung HS, Niu Y, Browse J, Howe GA (2009) Top hits in contemporary JAZ: an update on jasmonate signaling. Phytochemistry 70:1547–1559Google Scholar
  13. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  14. Dabrowska P, Boland W (2007) Iso-OPDA: an early precursor of cis-jasmone in plants? Chembiochem 8:2281–2285CrossRefPubMedGoogle Scholar
  15. Dabrowska P, Freitak D, Vogel H, Heckel DG, Boland W (2009) The phytohormone precursor OPDA is isomerized in the insect gut by a single, specific glutathione transferase. Proc Natl Acad Sci U SA 106:16304–16309CrossRefGoogle Scholar
  16. de Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580CrossRefPubMedGoogle Scholar
  17. De Vos M, Van Oosten VR, Van Pelt JA, Pozo MJ, Van Loon LC, Pieterse CMJ, Van Poecke RMP, Dicke M, Mueller MJ, Buchala AJ, Métraux J-P (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant-Microbe Interact 18:923–937CrossRefPubMedGoogle Scholar
  18. Devoto A, Ellis C, Magusin A, Chang HS, Chilcott C, Zhu T, Turner JG (2005) Expression profiling reveals COI1 to be a key regulator of genes involved in wound- and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions. Plant Mol Biol 58:497–513CrossRefPubMedGoogle Scholar
  19. Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716CrossRefPubMedGoogle Scholar
  20. Feys BJF, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751–759CrossRefPubMedGoogle Scholar
  21. Fode B, Siemsen T, Thurow C, Weigel R, Gatz C (2008) The Arabidopsis GRAS protein SCL14 interacts with class II TGA transcription factors and is essential for the activation of stress-inducible promoters. Plant Cell 20:3122–3135CrossRefPubMedGoogle Scholar
  22. Gallie DR, Lucas WJ, Walbot V (1989) Visualizing mRNA expression in plant protoplasts: factors influencing efficient mRNA uptake and translation. Plant Cell 1:301–311CrossRefPubMedGoogle Scholar
  23. Glazebrook J, Chen W, Estes B, Chang HS, Nawrath C, Métraux JP, Zhu T, Katagiri F (2003) Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J 34:217–228CrossRefPubMedGoogle Scholar
  24. Heil M (2004) Induction of two indirect defences benefits lima bean (Phaseolus lunatus, Fabaceae) in nature. J Chem Ecol 92:527–536Google Scholar
  25. Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61CrossRefPubMedGoogle Scholar
  26. James D (2005) Further field evaluation of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. J Chem Ecol 31:481–495CrossRefPubMedGoogle Scholar
  27. Jefferson RA, Kavanagh TA, Bevan MW (1987) Gus fusion: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907PubMedGoogle Scholar
  28. Kankainen M, Holm L (2004) POBO, transcription factor binding site verification with bootstrapping. Nucleic Acids Res 32:W222–W229CrossRefPubMedGoogle Scholar
  29. Kishimoto K, Matsu K, Ozawa R, Takabayashi J (2005) Volatile C6 aldehydes and allo-ocimene activate defence genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol 46:1093–1102CrossRefPubMedGoogle Scholar
  30. Koch T, Bandemer K, Boland W (1997) Biosynthesis of CJ: a pathway for the inactivation and the disposal of the plant stress hormone jasmonic acid to the gas phase? Helv Chim Acta 80:838–850CrossRefGoogle Scholar
  31. Kuroda H, Takahashi N, Shimada H, Seki M, Shinozaki K, Matsui M (2002) Classification and expression analysis of Arabidopsis F-box-containing protein genes. Plant Cell Physiol 43:1073–1085CrossRefPubMedGoogle Scholar
  32. Lou Y, Baldwin IT (2003) Manduca sexta recognition and resistance among allopolyploid Nicotiana host plants. Proc Natl Acad Sci USA 100:14581–14586CrossRefPubMedGoogle Scholar
  33. Loughrin JH, Manukian A, Heath RR, Tumlinson JH (1995) Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. J Chem Ecol 21:1217–1227CrossRefGoogle Scholar
  34. Luhua S, Ciftci-Yilmaz S, Harper J, Cushman J, Mittler R (2008) Enhanced tolerance to oxidative stress in transgenic Arabidopsis plants expressing proteins of unknown function. Plant Physiol 148:280–292CrossRefPubMedGoogle Scholar
  35. Moraes MC, Birkett MA, Gordon-Weeks R, Smart LE, Martin JL, Pye BJ, Bromilow R, Pickett JA (2008) CJ induces accumulation of defence compounds in wheat, Triticum aestivum. Phytochemistry 69:9–17CrossRefPubMedGoogle Scholar
  36. Mueller S, Hilbert B, Dueckershoff K, Roitsch T, Krischke M, Mueller MJ, Berger S (2008) General detoxification and stress responses are mediated by oxidized lipids through TGA transcription factors in Arabidopsis. Plant Cell 20:768–785CrossRefPubMedGoogle Scholar
  37. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue. Physiol Plant 15:473–497CrossRefGoogle Scholar
  38. Páre PW, Tumlinson JH (1997) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol 114:1161–1167PubMedGoogle Scholar
  39. Páre PW, Tumlinson JH (1999) Plant volatiles as a defence against insect herbivores. Plant Physiol 121:325–331CrossRefPubMedGoogle Scholar
  40. Pickett JA, Birkett MA, Moraes MCB, Bruce TJA, Chamberlain K, Gordon-Weeks R, Matthes MC, Napier JA, Smart LE, Wadhams LJ, Woodcock CM (2007) cis-Jasmone as allelopathic agent in inducing plant defence. Allelopathy J 19:109–117Google Scholar
  41. Röse USR, Tumlinson JH (2004) Volatiles released from cotton plants in response to Helicoverpa zea feeding damage on cotton flower buds. Planta 218:824–832CrossRefPubMedGoogle Scholar
  42. Röse USR, Tumlinson JH (2005) Systemic induction of volatile release in cotton: how specific is the signal to herbivory? Planta 222:327–335CrossRefPubMedGoogle Scholar
  43. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbour Laboratory Press, Cold Spring Harbour, NYGoogle Scholar
  44. Schaffer R, Landgraf J, Accerb M, Simon V, Larson M, Wisman E (2001) Microarray analysis of diurnal and circadian genes in Arabidopsis. Plant Cell 13:113–123CrossRefPubMedGoogle Scholar
  45. Schaller F (2001) Enzymes of the biosynthesis of octadecanoid-derived signalling molecules. J Exp Bot 52:11–13CrossRefPubMedGoogle Scholar
  46. Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377CrossRefPubMedGoogle Scholar
  47. Schlotzhauer WS, Pair SD, Horvat RJ (1996) Volatile constituents from the flowers of Japanese honeysuckle (Lonicera japonica). J Agric Food Chem 44:206–209CrossRefGoogle Scholar
  48. Schulze B, Dabrowska P, Boland W (2007) Rapid enzymatic isomerisation of 12-oxophytodienoic acid in the gut of Lepidopteran larvae. Chembiochem 8:208–216CrossRefPubMedGoogle Scholar
  49. Smith C, Liu X, Wang L, Liu X, Chen M-S, Starkey S, Bai J (2010) Aphid feeding activates expression of a transcriptome of oxylipin-based defense signals in wheat involved in resistance to herbivory. J Chem Ecol 36:260–276CrossRefPubMedGoogle Scholar
  50. Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127CrossRefPubMedGoogle Scholar
  51. Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89:6837–6840CrossRefPubMedGoogle Scholar
  52. Stintzi A, Weber H, Reymond P, Browse J, Farmer EE (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc Natl Acad Sci USA 98:12837–12842CrossRefPubMedGoogle Scholar
  53. Taki N, Sasaki-Sekimoto Y, Obayashi T, Kikuta A, Kobayashi K, Ainai T, Yagi K, Sakurai N, Suzuki H, Masuda T, Takamiya K, Shibata D, Kobayashi Y, Ohta H (2005) 12-Oxo-phytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis. Plant Physiol 139:1268–1283CrossRefPubMedGoogle Scholar
  54. Tanaka K, Uda Y, Ono Y, Nakagawa T, Suwa M, Yamaoka R, Touhara K (2009) Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Curr Biol 19:881–890CrossRefPubMedGoogle Scholar
  55. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI complex during jasmonate signalling. Nature 448:661–666CrossRefPubMedGoogle Scholar
  56. Turlings TC, Ton J (2006) Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Curr Opin Plant Biol 9:421–427CrossRefPubMedGoogle Scholar
  57. Turner SR, Somerville CR (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9:689–701CrossRefPubMedGoogle Scholar
  58. Umoru PA, Powell W, Clark SJ (1996) Effect of pirimicarb on the foraging behaviour of Diaeretiella rapae (Hymenoptera: Braconidae) on host-free and infested oilseed rape plants. Bull Entomol Res 86:193–201CrossRefGoogle Scholar
  59. Von Dahl CC, Baldwin IT (2004) Methyl jasmonate and CJ do not dispose of the herbivore-induced jasmonate burst in Nicotiana attenuate. Physiol Plant 120:474–481CrossRefGoogle Scholar
  60. Weber H, Chételat A, Reymond P, Farmer EE (2004) Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. Plant J 37:877–888CrossRefPubMedGoogle Scholar
  61. Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094CrossRefPubMedGoogle Scholar
  62. Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, Wang Z, Xie D (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21:2220–2236CrossRefPubMedGoogle Scholar
  63. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30:e15CrossRefPubMedGoogle Scholar
  64. Zhou JM, Trifa Y, Silva H, Pontier D, Lam E, Shah J, Klessig DF (2000) NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol Plant-Microbe Interact 13:191–202CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Michaela C. Matthes
    • 1
  • Toby J. A. Bruce
    • 1
  • Jurriaan Ton
    • 1
  • Paul J. Verrier
    • 2
  • John A. Pickett
    • 1
  • Johnathan A. Napier
    • 1
  1. 1.Biological Chemistry DepartmentRothamsted ResearchHarpendenUK
  2. 2.Biomathematics and Bioinformatics DepartmentRothamsted ResearchHarpendenUK

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