Biologia Plantarum

, Volume 50, Issue 1, pp 94–106

Early defence responses induced by two distinct elicitors derived from a Botrytis cinerea in grapevine leaves and cell suspensions

  • V. Repka
Article

Abstract

Two elicitors, termed herein as the botrycin and the cinerein, have been isolated from the crude mycelial cell wall and from culture filtrate preparations, respectively, of a fungal necrotrophic pathogen Botrytis cinerea (Pers. et Fries). In grapevine (Vitis vinifera L. cv. Limberger) both elicitors caused the formation of necrotic lesions that mimic a typical hypersensitive response and apoptosis-related events including protoplast condensation and DNA laddering. Infiltration of minute amounts of the respective elicitors into leaves stimulated a rapid transcriptional activation of genes encoding enzymes of the phenylpropanoid pathway. Cultured grapevine cells respond differentially to respective elicitors. Significant differences were demonstrated in the ability of botrycin and cinerein to induce ion fluxes across the plasma membrane and the production of reactive oxygen species. As demonstrated by immunokinase assays, both botrycin and cinerein activated specific and distinct MAP kinases indicating that grapevine cells that perceived elicitors generated a cascade of signals acting at local, short, and long distances. Using a highly parallel antibody microarray profiling approach, the timing, dynamics, and regulation of the expression of 97 specific genes in elicitor-treated cells of grapevine was analysed.

Additional key words

cell death Cucumis sativus hypersensitive response microarray profiling Nicotiana tabacum oxidative burst PR-gene expression protein phosphorylation run-off transcription Vitis vinifera 

Abbreviations

CHS

chalcone synthase

HIC

hydrophobic interaction chromatography

HRP

horseradish peroxidase

MAP

mitogen-activated protein kinase

MeJA

methyl jasmonate

NaF

sodium fluoride

NIA

necrosis inducing activity

PAL

phenylalanine ammonia-lyase

PCD

programmed cell death

PR

pathogenesis-related proteins

PRX

peroxidase

SA

salicylic acid

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson, A.J.: The molecular basis of plant resistance mechanisms.-In: Nester, E.W., Kosuge, T. (ed.): The Biology of Glycoproteins as Elicitors. Pp. 1–66. MacMillan Publishers, New York 1987.Google Scholar
  2. Asai, T., Stone, J., Heard, J.E., Kovtun, Y., Yorgey, P., Sheen, J., Ausubel, F.M.: Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylic acid-dependent signaling pathways.-Plant Cell 12: 1823–1835, 2000.CrossRefPubMedGoogle Scholar
  3. Baillieul, F., Genetet, I., Kopp, M., Sandrenan, P., Fritig, B., Kauffmann, S.: A new elicitor of the hypersensitive response in tobacco: a fungal glycoprotein elicits cell death, expression of defense genes, production of salicylic acid, and induction of systemic acquired resistance.-Plant J. 8: 551–560, 1995.CrossRefPubMedGoogle Scholar
  4. Boller, T.: Chemoperception of microbial signals in plant cells.-Annu. Rev. Plant Physiol. Plant mol. Biol. 46: 189–214, 1995.CrossRefGoogle Scholar
  5. Boller, T., Gehri, A., Mauch, F., Vogelli, U.: Chitinase in bean leaves: induction by ethylene, purification, properties, and possible function.-Planta 157: 22–31, 1983.CrossRefGoogle Scholar
  6. Bradford, M.M.: A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle of protein-dye binding.-Anal. Biochem. 72: 248–254, 1976.CrossRefPubMedGoogle Scholar
  7. Busam, G., Kassemeyer, H.-H., Matern, U.: Differential expression of chitinases in Vitis vinifera L. responding to systemic acquired resistance activators or fungal challenge.-Plant Physiol. 115: 1029–1038, 1997.PubMedGoogle Scholar
  8. Cardinale, F., Jonak, C., Ligterink, W., Niehaus, K., Boller, T., Hirt, H.: Differential activation of four specific MAPK pathways by distinct elicitors.-J. biol. Chem. 275: 36734–36740, 2000.CrossRefPubMedGoogle Scholar
  9. Corbin, D.R., Sauer, N., Lamb, C.J.: Differential regulation of a hydroxyproline-rich glycoprotein gene family in wounded and infected plants.-Mol. cell. Biol. 7: 4337–4344, 1987.PubMedGoogle Scholar
  10. De Jaegher, G., Boyer, N., Gaspar, T.: Thigmomorphogenesis in Bryonia dioica: changes in soluble and wall peroxidases, phenylalanine ammonia-lyase activity, cellulose, lignin content and monomeric constituents.-Plant Growth Regul. 3: 133–148, 1985.CrossRefGoogle Scholar
  11. De Jong, A.J., Hoeberichts, F.A., Yakimova, E.T., Maximova, E., Woltering, J.: Chemical-induced apoptotic cell death in tomato cells: involvement of caspase-like proteases.-Planta 211: 656–662, 2000.PubMedGoogle Scholar
  12. Delledonne, M., Xia, Y., Dixon, R.A., Lamb, C.J.: Nitric oxide functions in plant disease resistance.-Nature 394: 585–588, 1998.PubMedGoogle Scholar
  13. De Wit, P.J.G.M.: Fungal avirulence genes and plant resistance genes: Unraveling the molecular basis of gene-for-gene resistance.-Adv. Bot. Res. 21: 147–185, 1995.Google Scholar
  14. Dickman, M.B., Park, Y.K., Oltersdorf, T., Li, W., Clemente, T., French, R.: Abrogation of disease development in plants expressing animal antiapoptotic genes.-Proc. nat. Acad. Sci. USA 98: 6957–6962, 2001.CrossRefPubMedGoogle Scholar
  15. Dorey, S., Kopp, M., Geoffroy, P., Fritig, B., Kauffmann, S.: Hydrogen peroxide from the oxidative burst is neither necessary nor sufficient for hypersensitive cell death induction, phenylalanine ammonia-lyase stimulation, salicylic acid accumulation, or scopoletin consumption in cultured tobacco cells treated with elicitin.-Plant Physiol. 121: 163–171, 1999.CrossRefPubMedGoogle Scholar
  16. Ebel, J., Cosio, E. G.: Elicitors of plant defense responses.-Int. Rev. Cytol. 148: 1–36, 1994.Google Scholar
  17. Eisen, M.B., Spellman, P.T., Brown, P.O., Botstein, D.: Cluster analysis and display of genome-wide expression patterns.-Proc. nat. Acad. Sci. USA 95: 14863–14868, 1998.CrossRefPubMedGoogle Scholar
  18. Fritig, B., Legrand, M., Hirth, L.: Changes in the metabolism of phenolic compounds during the hypersensitive reaction of tobacco to TMV.-Virology, 47: 845–848, 1972.CrossRefPubMedGoogle Scholar
  19. Hammond-Kosack, K.E., Jones, J.D.G.: Resistance gene-dependent plant defense responses.-Plant Cell 8: 1773–1791, 1996.CrossRefPubMedGoogle Scholar
  20. Hedenfalk, I., Duggan, D., Chen, Y., Radmacher, M., Bittner, M., Simon, R., Meltzer, P., Gusterson, B., Esteller, M., Kallioniemi, P., Wilford, B., Borg, A., Trent, J.: Gene expression profiles in hereditary breast cancer.-N. Engl. J. Med. 344: 539–548, 2001.CrossRefPubMedGoogle Scholar
  21. Hinch, J.M., Clarke, A.E.: Callose formation in Zea mays as a response to infection with Phytophthora cinnamomi.-Physiol. Plant Pathol. 21: 113–124, 1982.CrossRefGoogle Scholar
  22. Hirt, H.: Multiple roles of MAP kinases in plant signal transduction.-Trends Plant Sci. 2: 11–15, 1997.CrossRefGoogle Scholar
  23. Hoch, H.C., Staples, R.C.: Signalling for infection structure formation in fungi.-In: Cole, G.T., Hoch, H.C. (ed.): The Fungal Spore and Disease Initiation in Plants and Animals. Pp. 25–42. Plenum Publishing, New York 1991.Google Scholar
  24. Jabs, T., Tschope, M., Colling, C., Hahlbrock, K., Scheel, D.: Elicitor-stimulated ion fluxes and O2 from the oxidative burst are essential components in triggering defense gene and phytoalexin synthesis in parsley.-Proc. nat. Acad. Sci. USA 94: 4800–4805, 1997.CrossRefPubMedGoogle Scholar
  25. Jacobs, A.K., Dry, I.B., Robinson, S.P.: Induction of different pathogenesis — related cDNAs in grapevine infected with powdery mildew and treated with ethephon.-Plant Pathol. 48: 325–336, 1999.CrossRefGoogle Scholar
  26. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4.-Nature 227: 680–685, 1970.CrossRefPubMedGoogle Scholar
  27. Lamb, C.J., Dixon, R.A.: Molecular communication in interactions between plants and microbial pathogens.-Annu. Rev. Plant Physiol. Plant mol. Biol. 41: 339–367, 1990.Google Scholar
  28. Lotan, R., Fluhr, R.: Function and regulated accumulation of plant pathogenesis-related proteins.-Symbiosis 8: 33–46, 1990.Google Scholar
  29. May, M.J., Hammond-Kosack, K.E., Jones, J.D.G.: Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the Cf-gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum.-Plant Physiol. 110: 1367–1379, 1996.PubMedGoogle Scholar
  30. Meskiene, I., Hirt, H.: MAP kinase pathways: molecular plug-and-play chips for the cell.-Plant mol. Biol. 42: 791–806, 2000.CrossRefPubMedGoogle Scholar
  31. Miller, J.C., Zhou, H., Kwekel, J., Cavallo, R., Burke, J., Butler, E.B., Teh, B.S., Haab, B.: Antibody microarray profiling of human prostate cancer sera: Antibody screening and identification of potential biomarkers.-Proteomics 3: 56–63, 2003.CrossRefPubMedGoogle Scholar
  32. Mittler, R., Lam, E.: Characterization of nuclease activities and DNA fragmentation induced upon hypersensitive response cell death and mechanical stress.-Plant mol. Biol. 34: 209–221, 1997.CrossRefPubMedGoogle Scholar
  33. Navarre, D.A., Wolpert, T.J.: Victorin induction of an apoptotic/senescence-like response in oats.-Plant Cell 11: 237–249, 1999.CrossRefPubMedGoogle Scholar
  34. Pena-Cortes, H., Albrecht, T., Prat, S., Weiler, W., Willmitzer, L.: Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis.-Planta 191: 123–128, 1993.Google Scholar
  35. Pena-Cortes, H., Sanchez-Serranno, J.J., Mertens, R., Willmitzer, L.: Abscisic acid is involved in the wound-induced expression of the proteinase inhibitor II gene in potato and tomato.-Proc. nat. Acad. Sci. USA 86: 9851–9855, 1989.PubMedGoogle Scholar
  36. Repka, V.: Elicitor-stimulated induction of defense mechanisms and defense gene activation in grapevine cell suspension cultures.-Biol. Plant. 44: 555–565, 2001.CrossRefGoogle Scholar
  37. Repka, V.: Hydrogen peroxide generated via the octadecanoid pathway is neither necessary nor sufficient for methyl jasmonate-induced hypersensitive cell death.-Biol. Plant. 45: 105–115, 2002a.CrossRefGoogle Scholar
  38. Repka, V.: Botrycin and cinerein, two structurally and functionally distinct elicitors of defense responses from a grapevine fungal necrotroph Botrytis cinerea (PERS. et FRIES).-Bull. OIV 76: 175–184, 2002b.Google Scholar
  39. Repka, V.: Chlorophyll-deficient mutant in oak (Quercus petraea L.) displays an accelerated hypersensitive-like cell death and an enhanced resistance to powdery mildew disease.-Photosynthetica 40: 183–193, 2002c.CrossRefGoogle Scholar
  40. Repka, V., Fischerova, I., Canigova, K.: Expression of cucumber stress-related anionic peroxidases during flower development or a cryptic infective process.-Biol. Plant. 38: 585–596, 1996.Google Scholar
  41. Repka, V., Fischerova, I., Silharova, K.: Biological activity of the elicitor released from mycelium of a grapevine isolate of the necrotrophic fungus Botrytis cinerea.-Vitis 40: 205–212, 2001b.Google Scholar
  42. Repka, V., Kubikova, J., Fischerova, I.: Immunodetection of PR-1-like proteins in grapevine leaves infected with Oidium tuckeri and in elicited suspension cell cultures.-Vitis 39: 123–127, 2000.Google Scholar
  43. Repka, V., Fischerova, I., Silharova, K.: Methyl jasmonate induces a hypersensensitive-like response of grapevine in the absence of avirulent pathogens.-Vitis 40: 5–10, 2001a.Google Scholar
  44. Repka, V., Slovakova, L.: Purification, characterization and accumulation of three virus-induced cucumber peroxidases.-Biol. Plant. 36: 121–132, 1994.Google Scholar
  45. Romeis, T., Piedras, P., Zhang, S., Klessig, D.F., Hirt, H., Jones, J.D.: Rapid Avr-D and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves. Convergence of resistance gene, elicitor, wound, and salicylate responses.-Plant Cell 11: 273–288, 1999.CrossRefPubMedGoogle Scholar
  46. Ryerson, D.E., Heath, M.C.: Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments.-Plant Cell 8: 393–402, 1996.CrossRefPubMedGoogle Scholar
  47. Schraudner, M., Moeder, W., Wiese, C., Van Camp, W., Inze, D., Langebartels, C., Sandermann, H.: Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3.-Plant J. 16: 235–245, 1998.CrossRefGoogle Scholar
  48. Snyder, B.A., Nicholson, R.L.: Synthesis of phytoalexins in sorghum as a site-specific response to fungal ingress.-Science 248: 1637–1639, 1990.PubMedGoogle Scholar
  49. Stetkova, D., Repka, V.: 14-3-3 proteins: magic numbers in molecular biology.-Biol. Lett. 66: 161–186, 2001.Google Scholar
  50. Takahashi, M., Rhodes, D., Furge, K.A., Kanayama, H., Kagawa, S., Haab, B.B., Teh, B.: Gene expression profiling of clear renal cell carcinoma: gene identification and prognostic classification.-Proc. nat. Acad. Sci. USA 98: 9754–9759, 2001.PubMedGoogle Scholar
  51. Turner, J.G., Novacky, A.: The quantitative relation between plant and bacterial cells involved in the hypersensitive response.-Phytopathology 64: 885–890, 1974.CrossRefGoogle Scholar
  52. Wang, M., Hoekstra, S., Bergen, S., Lamers, G.E.M., Oppendijk, B.J., Heijden, M.W., Priester, W., Schilperoort, R.A.: Apoptosis in developing anthers and the role of ABA in this process during androgenesis in Hordeum vulgare L.-Plant mol. Biol. 39: 489–501, 1999.CrossRefPubMedGoogle Scholar
  53. Xu, P., Roosnick, M.J.: Cucumber mosiac virus D satellite RNA-induced programmed cell death in tomato.-Plant Cell 12: 1079–1092, 2000.CrossRefPubMedGoogle Scholar
  54. Xu, Y., Hanson, M.R.: Programmed cell death during pollination-induced petal senescence in petunia.-Plant Physiol. 122: 1323–1333, 2000.CrossRefPubMedGoogle Scholar
  55. Yano, A., Suzuki, K., Uchimya, H., Shinshi, H.: Induction of hypersensitive cell death by a fungal protein in cultures of tobacco cells.-Mol. Plant-Microb. Interact. 11: 115–123, 1998.CrossRefGoogle Scholar
  56. Zhang, S., Klessig, D.F.: Salicylic acid activates a 48-kD MAP kinase in tobacco.-Plant Cell 9: 809–824, 1997.CrossRefPubMedGoogle Scholar

Copyright information

© Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Praha 2006

Authors and Affiliations

  • V. Repka
    • 1
  1. 1.Laboratory of Molecular Biology and VirologyResearch Institute of Viticulture and Enology (CRIVE)BratislavaSlovakia

Personalised recommendations