biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 50:94-106, 2006 | DOI: 10.1007/s10535-005-0080-z

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

V. Repka1
1 Laboratory of Molecular Biology and Virology, Research Institute of Viticulture and Enology (CRIVE), Bratislava, Slovakia

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.

Keywords: cell death; Cucumis sativus; hypersensitive response; microarray profiling; Nicotiana tabacum; oxidative burst; PR-gene expression; protein phosphorylation; run-off transcription; Vitis vinifera
Subjects: antioxidants, antioxidative enzymes; botrycin; Botrytis cinerea; cell death, programmed; cell wall, mycelial; cinerein; cucumber; Cucumis sativus; defence response; early defence responses; grapevine; in vitro culture, cell suspension cultures; jasmonic acid, jasmonate, methyl jasmonate; Nicotiana tabacum; pathogenesis-related proteins (PR); peroxidase; phenylalanine ammonia lyase; proteins; salicylic acid; tobacco; Vitis vinifera; Western blot analysis

Received: April 19, 2004; Accepted: May 9, 2005; Published: March 1, 2006  Show citation

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Repka, V. (2006). Early defence responses induced by two distinct elicitors derived from a Botrytis cinerea in grapevine leaves and cell suspensions. Biologia plantarum50(1), 94-106. doi: 10.1007/s10535-005-0080-z
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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.
  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. Go to original source...
  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. Go to original source...
  4. Boller, T.: Chemoperception of microbial signals in plant cells.-Annu. Rev. Plant Physiol. Plant mol. Biol. 46: 189-214, 1995. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  12. Delledonne, M., Xia, Y., Dixon, R.A., Lamb, C.J.: Nitric oxide functions in plant disease resistance.-Nature 394: 585-588, 1998. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  16. Ebel, J., Cosio, E. G.: Elicitors of plant defense responses.-Int. Rev. Cytol. 148: 1-36, 1994. Go to original source...
  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. Go to original source...
  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. Go to original source...
  19. Hammond-Kosack, K.E., Jones, J.D.G.: Resistance gene-dependent plant defense responses.-Plant Cell 8: 1773-1791, 1996. Go to original source...
  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. Go to original source...
  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. Go to original source...
  22. Hirt, H.: Multiple roles of MAP kinases in plant signal transduction.-Trends Plant Sci. 2: 11-15, 1997. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  26. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4.-Nature 227: 680-685, 1970. Go to original source...
  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. Go to original source...
  28. Lotan, R., Fluhr, R.: Function and regulated accumulation of plant pathogenesis-related proteins.-Symbiosis 8: 33-46, 1990.
  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. Go to original source...
  30. Meskiene, I., Hirt, H.: MAP kinase pathways: molecular plug-and-play chips for the cell.-Plant mol. Biol. 42: 791-806, 2000. Go to original source...
  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. Go to original source...
  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. Go to original source...
  33. Navarre, D.A., Wolpert, T.J.: Victorin induction of an apoptotic/senescence-like response in oats.-Plant Cell 11: 237-249, 1999. Go to original source...
  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. Go to original source...
  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. Go to original source...
  36. Repka, V.: Elicitor-stimulated induction of defense mechanisms and defense gene activation in grapevine cell suspension cultures.-Biol. Plant. 44: 555-565, 2001. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  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. Go to original source...
  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.
  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.
  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.
  44. Repka, V., Slovakova, L.: Purification, characterization and accumulation of three virus-induced cucumber peroxidases.-Biol. Plant. 36: 121-132, 1994. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  49. Stetkova, D., Repka, V.: 14-3-3 proteins: magic numbers in molecular biology.-Biol. Lett. 66: 161-186, 2001.
  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. Go to original source...
  51. Turner, J.G., Novacky, A.: The quantitative relation between plant and bacterial cells involved in the hypersensitive response.-Phytopathology 64: 885-890, 1974. Go to original source...
  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. Go to original source...
  53. Xu, P., Roosnick, M.J.: Cucumber mosiac virus D satellite RNA-induced programmed cell death in tomato.-Plant Cell 12: 1079-1092, 2000. Go to original source...
  54. Xu, Y., Hanson, M.R.: Programmed cell death during pollination-induced petal senescence in petunia.-Plant Physiol. 122: 1323-1333, 2000. Go to original source...
  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. Go to original source...
  56. Zhang, S., Klessig, D.F.: Salicylic acid activates a 48-kD MAP kinase in tobacco.-Plant Cell 9: 809-824, 1997. Go to original source...