, Volume 254, Issue 1, pp 271–283 | Cite as

Jasmonates are induced by the PAMP flg22 but not the cell death-inducing elicitor Harpin in Vitis rupestris

  • Xiaoli Chang
  • Mitsunori Seo
  • Yumiko Takebayashi
  • Yuji Kamiya
  • Michael Riemann
  • Peter Nick
Original Article


Plants employ two layers of defence that differ with respect to cell death: pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and effector-triggered immunity (ETI). In our previous work, we have comparatively mapped the molecular events in a cell system derived from the wild American grape Vitis rupestris, where cell death-independent defence can be triggered by PAMP flg22, whereas the elicitor Harpin activates a cell death-related ETI-like response. Both defence responses overlapped with respect to early events, such as calcium influx, apoplastic alkalinisation, oxidative burst, mitogen-activated protein kinase (MAPK) signalling, activation of defence-related genes and accumulation of phytoalexins. However, timing and amplitude of early signals differed. In the current study, we address the role of jasmonates (JAs) as key signalling compounds in hypersensitive cell death. We find, in V. rupestris, that jasmonic acid and its bioactive conjugate jasmonoyl-isoleucine (JA-Ile) rapidly accumulate in response to flg22 but not in response to Harpin. However, Harpin can induce programmed cell death, whereas exogenous methyl jasmonate (MeJA) fails to do so, although both signals induce a similar response of defence genes. Also in a second cell line from V. vinifera cv. ‘Pinot Noir’, where Harpin cannot activate cell death and where flg22 fails to induce JA and JA-Ile, defence genes are activated in a similar manner. These findings indicate that the signal pathway culminating in cell death must act independently from the events culminating in the accumulation of toxic stilbenes.


Defence signalling Effector-triggered immunity (ETI) Jasmonic acid (JA) PAMP-triggered immunity (PTI) Vitis 

Supplementary material

709_2016_941_MOESM1_ESM.doc (89 kb)
ESM 1(DOC 89 kb)


  1. An C, Mou Z (2011) Salicylic acid and its function in plant immunity. J Integr Plant Biol 53(6):412–428CrossRefPubMedGoogle Scholar
  2. Alonso-Villaverde V, Voinesco F, Viret O, Spring JL, Gindro K (2011) The effectiveness of stilbenes in resistant Vitaceae: ultrastructural and biochemical events during Plasmopara viticola infection process. Plant Physiol Biochem 49:265–274CrossRefPubMedGoogle Scholar
  3. Aumont V, Larronde F, Richard T, Budzinski H, Decendit A, Deffieux G, Krisa S, Mérillon JM (2004) Production of highly 13C-labeled polyphenols in Vitis vinifera cell bioreactor cultures. J Biotechnol 109:287–294CrossRefPubMedGoogle Scholar
  4. Belhadj A, Telef N, Saigne C, Cluzet S, Barrieu F, Hamdi S, Mérillon JM (2008) Effect of methyl jasmonate in combination with carbohydrates on gene expression of PR proteins, stilbene and anthocyanin accumulation in grapevine cell cultures. Plant Physiol Biochem 46:493–499CrossRefPubMedGoogle Scholar
  5. Bernoux M, Ellis JG, Dodds PN (2011) New insights in plant immunity signaling activation. Curr Opin Plant Biol 14:512–518CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bittel P, Robatzek S (2007) Microbe-associated molecular patterns (MAMPs) probe plant immunity. Curr Opin Plant Biol 10:335–341CrossRefPubMedGoogle Scholar
  7. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406CrossRefPubMedGoogle Scholar
  8. Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43:545–580CrossRefPubMedGoogle Scholar
  9. Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60:183–205CrossRefPubMedGoogle Scholar
  10. Chang X, Heene E, Qiao F, Nick P (2011) The phytoalexin resveratrol regulates the initiation of hypersensitive cell death in Vitis cell. PLoS ONE 6:e26405CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chang X, Nick P (2012) Defence signalling triggered by Flg22 and Harpin is integrated into a different stilbene output in Vitis cells. PLoS ONE 7, e40446CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500CrossRefPubMedGoogle Scholar
  13. Chini A, Boter M, Solano R (2009) Plant oxylipins: COI1/JAZs/MYC2 as the core jasmonic acid-signalling module. FEBS J 276:4682–4692CrossRefPubMedGoogle Scholar
  14. Dong X (2004) NPR1, all things considered. Curr Opin Plant Biol 7:547–552CrossRefPubMedGoogle Scholar
  15. Donnez D, Kim KH, Antoine S, Conreux A, De Luca V, Jeandet P, Clément C, Courot E (2011) Bioproduction of resveratrol and viniferins by an elicited grapevine cell culture in a 2L stirred bioreactor. Process Biochem 46:1056–1062CrossRefGoogle Scholar
  16. Duan D, Halter D, Baltenweck R, Tisch C, Tröster V, Kortekamp A, Hugueney P, Nick P (2015) Genetic diversity of stilbene metabolism in Vitis sylvestris. J Exp Bot 66(11):3243–3257Google Scholar
  17. Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265–276CrossRefPubMedGoogle Scholar
  18. Frescher E (2007) Jasmonates in cancer therapy. Cancer Lett 245:1–10CrossRefGoogle Scholar
  19. Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350CrossRefPubMedGoogle Scholar
  20. Gaff DF, Okong’O-Ogola O (1971) The use of non-permeating pigments for testing the survival of cells. J Exp Bot 22:756–758CrossRefGoogle Scholar
  21. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227CrossRefPubMedGoogle Scholar
  22. Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011CrossRefPubMedGoogle Scholar
  23. Grant M, Lamb C (2006) Systemic immunity. Curr Opin Plant Biol 9:414–420CrossRefPubMedGoogle Scholar
  24. Heitz T, Widemann E, Lugan R, Miesch L, Ullmann P, Désaubry L, Holder E, Grausem B, Kandel S, Miesch M, Werck-Reichhart D, Pinot F (2012) Cytochromes P45 CYP94C1 and CYP94B3 catalyze two successive oxidation steps of plant hormone Jasmonoyl-isoleucine for catabolic turnover. J Biol Chem 287:6296–6306CrossRefPubMedPubMedCentralGoogle Scholar
  25. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66CrossRefPubMedGoogle Scholar
  26. Ismail A, Riemann M, Nick Peter (2012) The jasmonate pathway mediates salt tolerance in grapevines. J Exp Bot 63(5):2127–2139Google Scholar
  27. Ismail A, Seo M, Takebayashi Y, Kamiya Y, Eiche E, Nick P (2014a) Salt adaptation requires efficient fine-tuning of Jasmonate signalling. Protoplasma 251:881–898CrossRefPubMedGoogle Scholar
  28. Ismail A, Takeda S, Nick P (2014b) Life and death under salt stress: sam players, different timing? J Exp Bot 65(12):2963–2979CrossRefPubMedGoogle Scholar
  29. Ismail A, Seo M, Takebayashi Y, Kamiya Y, Nick P (2015) A Balanced JA/ABA status might correlate with adaptation to osmotic stress in Vitis cells. J Plant Physiol 185:57–64CrossRefPubMedGoogle Scholar
  30. Jaillais Y, Chory J (2010) Unraveling the paradoxes of plant hormone signaling integration. Nat Struct Mol Biol 17:642–645CrossRefPubMedPubMedCentralGoogle Scholar
  31. Jeandet P, Douillet-Breuil AC, Bessis R, Debord S, Sbaghi M, Adrian M (2002) Phytoalexins from the Vitaceae: biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. J Agric Food Chem 50:2731–2741CrossRefPubMedGoogle Scholar
  32. Jeworutzki E, Roeflsema MR, Anschütz U, Krol E, Elzenga JT, Felix G, Boller T, Hedrich R, Becker D (2010) Early signaling through the Arabidopsis pattern recognition receptor FLS2 and EFR involves Ca2+-associated opening of plasma membrane anion channels. Plant J 62:367–378CrossRefPubMedGoogle Scholar
  33. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329CrossRefPubMedGoogle Scholar
  34. Jovanović AM, Durst S, Nick P (2010) Plant cell division is specifically affected by nitrotyrosine. J Exp Bot 61:901–909CrossRefPubMedGoogle Scholar
  35. Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229CrossRefPubMedGoogle Scholar
  36. Kazan K, Manners JM (2008) Jasmonate signaling: toward an integrated view. Plant Physiol 146:1459–1468CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kenton P, Mur LA, Atzorn R, Wasternack C, Draper J (1999) (−)-Jasmonic acid accumulation in tobacco hypersensitive response lesions. Mol Plant Microbe Interact 12:74–78CrossRefGoogle Scholar
  38. Kortekamp A (2006) Expression analysis of defence-related genes in grapevine leaves after inoculation with a host, a nonhost pathogen. Plant Physiol Biochem 44:58–67Google Scholar
  39. Krisa S, Larronde F, Budzinski H, Decendit A, Deffieux G, Mérillon JM (1999) Stilbene production by Vitis vinifera cell suspension cultures: methyl jasmonate induction and 13c biolabeling. J Nat Prod 62:1688–1690CrossRefGoogle Scholar
  40. Le Henanff G, Heitz T, Mestre P, Mutterer J, Walter B, Chong J (2009) Characterization of Vitis vinifera NPR1 homologs involved in the regulation of Pathogenesis-Related gene expression. BMC Plant Biol 9:54Google Scholar
  41. Mishina TE, Zeier J (2007) Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J 50:500–513CrossRefPubMedGoogle Scholar
  42. Nick P, Heuing A, Ehmann B (2000) Plant chaperonins: a role in microtubule-dependent wall-formation? Protoplasma 211:234–244CrossRefGoogle Scholar
  43. Nürnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266CrossRefPubMedGoogle Scholar
  44. Nürnberger T, Lipka V (2005) Nonhost resistance in plants: new insights into an old phenomenon. Mol Plant Pathol 6:335–345CrossRefPubMedGoogle Scholar
  45. Pauwels L, Inzé D, Goossens A (2009) Jasmonate-inducible gene: what does it mean? Trends Plant Sci 14:87–91CrossRefPubMedGoogle Scholar
  46. Pezet R, Perret C, Jean-Denis JB, Tabacchi R, Gindro K, Viret O (2003) δ-viniferin, a resveratrol dehydrodimer: one of the major stilbenes synthesized by stressed grapevine leaves. J Agric Food Chem 51:5488–5492CrossRefPubMedGoogle Scholar
  47. Pezet R, Gindro K, Viret O, Richter H (2004a) Effects of resveratrol, viniferins, pterostilbene on Plasmopara viticola zoospore mobility, disease development. Vitis 43:145–148Google Scholar
  48. Pezet R, Gindro K, Viret O, Spring JL (2004b) Glycosylation and oxidative dimerization of resveratrol are respectively associated to sensitivity and resistance of grapevine cultivars to downy mildew. Physiol Mol Plant P 65:297–303CrossRefGoogle Scholar
  49. Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316CrossRefPubMedGoogle Scholar
  50. Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521CrossRefPubMedGoogle Scholar
  51. Qiao F, Chang X, Nick P (2010) The cytoskeleton enhances gene expression in the response to the Harpin elicitor in grapevine. J Exp Bot 61:4021–4031CrossRefPubMedPubMedCentralGoogle Scholar
  52. Reid KE, Olsson N, Schlosser J, Peng F, Lund ST (2006) An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol 6:27Google Scholar
  53. Repka V (2001) Methyl jasmonate induces a hypersensitive-like response of grapevine in the absence of avirulent pathogens. Vitis 40:5–10Google Scholar
  54. Repka V, Fischerová I, Šilhárová K (2004) Methyl jasmonate is a potent elicitor of multiple defense responses in grapevine leaves and cell suspension cultures. Biol Plant 48:273–283CrossRefGoogle Scholar
  55. Repka V, Čarná M, Pavlovkin J (2013) Methyl jasmonate-induced cell death in grapevine requires both lipoxygenase activity and functional octadecanoid biosynthetic pathway. Biologia 68:896–903CrossRefGoogle Scholar
  56. Robatzek S (2014) Endocytosis: at the crossroads of pattern recognition immune receptors and pathogen effectors. Plant Cell Monogr 22:273–297CrossRefGoogle Scholar
  57. Seibicke T (2002) Untersuchungen zur induzierten Resistenz a Vitis spec. PhD thesis. University of FreiburgGoogle Scholar
  58. Seo HS, Song JT, Cheong JJ, Lee YH, Lee YW, Hwang I, Lee JS, Choi YD (2001) Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. PNAS 98:4788–4793CrossRefPubMedPubMedCentralGoogle Scholar
  59. Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Métraux JP, Brown R, Kazan K, Van Loon LC, Dong X, Pieterse CM (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770CrossRefPubMedPubMedCentralGoogle Scholar
  60. Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127CrossRefPubMedPubMedCentralGoogle Scholar
  61. Tassoni A, Fornalè S, Franceschetti M, Musiani F, Michael AJ, Perry B, Bagni N (2005) Jasmonates and Na-orthovanadate promote resveratrol production in Vitis vinifera cv. Barbera cell cultures. New Phytol 166:895–905CrossRefPubMedGoogle Scholar
  62. Thomma BP, Nürnberger T, Joosten MH (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15CrossRefPubMedPubMedCentralGoogle Scholar
  63. Tsuda K, Sato M, Glazebrook J, Cohen JD, Katagiri F (2008) Interplay between MAMP-triggered and SA-mediated defense responses. Plant J 53(5):763–775CrossRefPubMedGoogle Scholar
  64. Tsuda K, Katagiri F (2010) Comparing signalling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13:459–465CrossRefPubMedGoogle Scholar
  65. Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F (2009) Network properties of robust immunity in plants. PLoS Genet 5, e1000772CrossRefPubMedPubMedCentralGoogle Scholar
  66. Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206CrossRefPubMedGoogle Scholar
  67. Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot Lond 111:1021–1058CrossRefGoogle Scholar
  68. Widemann E, Miesch L, Lugan R, Holder E, Heinrich C, Aubert Y, Miesch M, Pinot F, Heitz T (2013) The amidohydrolases IAR3 and ILL6 contribute to Jasmonoyl-isoleucine hormone turnover and generate 12-hydroxyjasmonic acid upon wounding in Arabidopsis leaves. J Biol Chem 288:31701–31714CrossRefPubMedPubMedCentralGoogle Scholar
  69. Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C, Panstruga R, Ohsumi Y, Shirasu K (2009) Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signalling during senescence and the innate immune response in Arabidopsis. Plant Cell 21:2914–2927CrossRefPubMedPubMedCentralGoogle Scholar
  70. Yi SY, Shirasu K, Moon JS, Lee S, Kwon S (2014) The activated SA and JA signaling pathways have an influence on flg22-triggered oxidative burst and callose deposition. PLoS ONE 9(2), e88951CrossRefPubMedPubMedCentralGoogle Scholar
  71. Zhang L, Xing D (2008) Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death. Plant Cell Physiol 49:1092–1111CrossRefPubMedGoogle Scholar
  72. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  • Xiaoli Chang
    • 1
    • 3
  • Mitsunori Seo
    • 2
  • Yumiko Takebayashi
    • 2
  • Yuji Kamiya
    • 2
  • Michael Riemann
    • 3
  • Peter Nick
    • 3
  1. 1.Department of Plant Pathology, Agricultural CollegeSichuan Agricultural UniversityChengduPeople’s Republic of China
  2. 2.RIKEN Center for Sustainable Resource ScienceYokohamaJapan
  3. 3.Molecular Cell Biology, Botanical InstituteKarlsruhe Institute of TechnologyKarlsruheGermany

Personalised recommendations