Mycorrhiza-induced changes in disease severity and PR protein expression in tobacco leaves

Molecular Plant-Microbe Interactions

Volumn 12, Issue 11, 1999, Pages 1000-1007

  Shaul, Orna ^a   Galili, Shmuel ^a   Volpin, Hanne ^a   Ginzberg, Idit ^a   Elad, Yigal ^a   Chet, Ilan ^b   Kapulnik, Yoram ^a  

^a VOLCANI CENTER   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

(1,2,3) thiadiazole 7 carbothioic acid S methyl ester (BTH); 2,6 dichloroisonicotinic acid (INA); Chitinase; Symbiosis; Thiamine; UV

Indexed keywords

PROTEIN EXPRESSION; TOBACCO MOSAIC VIRUS; VIRULENCE;

ARBUSCULAR MYCORRHIZAE; BOTRYOTINIA FUCKELIANA; BOTRYTIS; BOTRYTIS CINEREA; FUNGI; GLOMUS INTRARADICES; MYCORRHIZAE; NICOTIANA TABACUM; TABACUM; TOBACCO MOSAIC VIRUS;

EID: 0032755361     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.1999.12.11.1000     Document Type: Article

References (54)

1. Alexander, D., Goodman, R. M., Gut-Rella, M., Glascock, C., Weymann, K., Friedrich, L., Maddox, D., Ahl-Goy, P., Luntz, T., Ward, E., and Ryals, J. 1993. Increased tolerance to two oomycetes pathogens in transgenic tobacco expressing pathogenesis related protein 1a. Proc. Natl. Acad. Sci. USA 90:7327-7331.
2. Allen, M. F., Moore, T. S., Jr., and Christensen, M. 1980. Phytohormone changes in Bouteloua gracilis by vesicular-arbuscular mycorrhizae: I. Cytokinin increases in host plant. Can. J. Bot. 58:371-374.
3. Allen, M. F., Moore, T. S., Jr., and Christensen, M. 1982. Phytohormone changes in Bouteloua gracilis infected by vesicular-arbuscular mycorrhizae. II. Altered levels of gibberellin-like substances and abscisic-acid in the host plant. Can. J. Bot. 60:486-471.
4. Bol, J. F., Linthorst, J. H., and Cornelissen, B. J. C. 1990. Plant pathogenesis-related proteins induced by virus infection. Annu. Rev. Phytopathol. 28:113-138.
5. Bonfante-Fasolo, P. 1987. Vesicular-arbuscular mycorrhizae: Fungus-plant interactions at the cellular level. Symbiosis 3:249-268.
6. Bonfante-Fasolo, P., and Perotto, S. 1992. Plants and endomycorrhizal fungi: The cellular and molecular basis of their interaction. Pages 445-470 in: Molecular Signals in Plant-Microbe Communications. D. P. Verma, ed. CRC, Boca Raton, FL.
7. Brederode, F. T., Linthorst, H. J. M., and Bol, J. F. 1991. Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Mol. Biol. 17:1117-1125.
8. Broglie, K., Chet, I., Holliday, M., Cressman, R., and Broglie, R. 1991. Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254:1194-1197.
9. Conrath, U., Silva, H., and Klessing, D. F. 1997. Protein dephosphorylation mediates salicylic acid-induced expression of PR-1 genes in tobacco. Plant J. 11:747-757.
10. Danneberg, G., Latus, C., Zimmer, W., Hundeshagen, B., Schneider-Poetsch, H. J., and Bothe, H. 1992. Influence of vesicular-arbuscular mycorrhiza on phytohormone balances in maize (Zea mays L). J. Plant Physiol. 141:33-39.
11. David, R., Itzhaki, H., Ginzberg, I., Gafni, Y., Galili, G., and Kapulnik, Y. 1998. Suppression of tobacco basic chitinase gene expression in response to colonization by the arbuscular mycorrhizal fungus Glomus intraradices. Mol. Plant-Microbe Interact. 11:489-497.
12. Dehne, H. W. 1982. Interaction between vesicular-arbuscular mycorrhizal fungi and plant pathogens. Phytopathology 72:1115-1119.
13. Dixon, R. K., Garrett, H. E., and Cox, G. S. 1988. Cytokinins in the root pressure exudate of Citrus jambhiri Lush colonized by vesicular-arbuscular mycorrhizae. Tree Physiol. 4:9-18.
14. Drüge, U., and Schönbeck, F. 1992. Effect of vesicular mycorrhizal infection on transpiration, phytosynthesis and growth of falx (Linum usitatissimum L.) in relation to cytokinin levels. J. Plant Physiol. 141: 40-48.
15. Elad, Y. 1988. Scanning electron microscopy study of parasitism of Botrytis cinerea on flower and fruits of cucumber. Trans. Br. Mycol. Soc. 91:185-190.
16. Elad, Y. 1995. Responses of plants to infection by Botrytis cinerea and novel means involved in reducing their susceptibility to infection. Biol. Rev. 72:381-422.
17. Elad, Y., Köhl, J., and Fokkema, N. J. 1994. Control of infection and sporulation of Botrytis cinerea on bean and tomato by saprophytic yeasts. Phytopathology 84:1193-1200.
18. Fieschi, M., Alloatti, G., Sacco, S., and Berta, G. 1992. Membrane potential hyperpolarization in vesicular arbuscular mycorrhizae of Allium porrum L.: A non-nutritional long-distance effect of the fungus. Protoplasma 168:136-140.
19. Friedrich, L., Lawton, K., Ruess, W., Masner, P., Specker, N., Gut-Rella, M., Meier, B., Dincher, S., Staub, T., Uknes, S., Métraux, J.-P., Kessmann, H., and Ryals, J. 1996. A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J. 10:61-70.
20. Gaffhey, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H., and Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261: 754-756.
21. Ginzberg, I., David, R., Shaul, O., Elad, Y., Wininger, S., Ben-Dor, B., Badani, H., Fang, Y., van Rhijn, P., Li, Y., Hirsch, A. M., and Kapulnik, Y. 1998. Glomus intraradices colonization regulates gene expression in tobacco plants. Symbiosis 24:145-157.
22. Harley, J. L., and Smith, S. E. 1983. Mycorrhizal Symbiosis. Academic, London.
23. Heitz, T., Segond, S., Kauffmann, S., Geoffroy, P., Prasad, V., Brunner, F., Fritig, B., and Legrand, M. 1994. Molecular characterization of a novel tobacco pathogenesis-related (PR) protein: A new plant chitinase/lysozyme. Mol. Gen. Genet. 245:246-254.
24. Johnson, C. M., Stout, P. R., Broyer, T. C., and Carlton, A. B. 1957. Comparative chlorine requirements of different plant species. Plant Soil 4:337.
25. Kapulnik, Y., Volpin, H., Itzhaki, H., Ganon, D., Galili, S., David, R., Shaul, O., Elad, Y., Chet, I., and Okon, Y. 1996. Suppression of defense responses in mycorrhizal alfalfa and tobacco roots. New Phytol. 133:59-64.
26. Kapulnik, Y., Volpin, H., and Palinski, W. 1993. Signals in plant vesicular-arbuscular mycorrhizal fungal symbiosis. Pages 142-152 in: Plant Signals in Interactions with Other Organisms. J. Schultz and I. Raskin, eds. American Society of Plant Physiologists, Rockville, MD.
27. Kúc, J. 1982. Induced immunity to plant disease. BioScience 32:845-860.
28. Lambais, M. R., and Mehdy, M. C. 1993. Suppression of endochitinase, β-1,3,-endoglucanase, and chalcone isomerase expression in bean vesicular-arbuscular mycorrhizal roots under different soil phosphate conditions. Mol. Plant-Microbe Interact. 6:75-83.
29. Lambais, M. R., and Mehdy, M. C. 1994. Differential expression of defense-related genes in arbuscular mycorrhizae. Can. J. Bot. 73:S533-S540.
30. Lawton, K., Ward, E., Payne, G., Moyer, M., and Ryals, J. 1992. Acidic and basic class I chitinase mRNA accumulation in response to TMV infection of tobacco. Plant Biol. 19:735-743.
31. Linderman, R. G. 1994. Role of VAM fungi in biocontrol. Pages 1-27 in: Mycorrhizae and Plant Health. F. L. Pfleger and R. G. Linderman, eds. American Phytopathological Society, St. Paul, MN.
32. Liu, D., Raghothama, K. G., Hasegawa, P., and Bressan, R. 1994. Osmotin overexpression in potato delays development of disease symptoms. Proc. Natl. Acad. Sci. USA 91:1888-1892.
33. Malamy, J., Carr, J. P., Klessing, D. F., and Raskin, I. 1990. Salicylic acid: A likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002-1004.
34. Métraux, J.-P., and Boller, T. 1986. Local and systemic induction of chitinase in cucumber plants in response to viral, bacterial and fungal infections. Physiol. Mol. Plant Pathol. 28:161-169.
35. Meyer, J., and Dehne, H.-W. 1986. The influence of VA mycorrhizae on biotrophic leaf pathogens. Mycorrhizae: Physiology and genetics. 1st ESM/1st SEM. INRA, Paris.
36. Payne, G., Middlesteadt, W., Williams, S., Desai, N., Park, T. D., Dincher, S., Carnes, M., and Ryals, J. 1988. Isolation and nucleotide sequence of a novel cDNA clone encoding the major form of pathogenesis-related protein R. Plant Mol. Biol. 11:223-224.
37. Ross, A. F. 1961. Systemic acquired resistance induced by localized virus infection in plants. Virology 14:340-358.
38. Ryals, J., Uknes, S., and Ward, E. 1994. Systemic acquired resistance. Plant Physiol. 104:1109-1112.
39. Sambrook, J., Fritsch, E. F., and Maniatis, T. A. 1989. Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
40. Schönbeck, F., and Dehne, H. W. 1979. The influence of endotrophic mycorrhiza on plant diseases. 4. Fungal parasites on aerial plant parts, Olpidium brassicae, TMV. Z. Pflanzenkrankh. Pflanzenschutz. 86: 103-107.
41. Shinshi, H., Mohnen, D., and Meins, F., Jr. 1987. Regulation of a plant pathogenesis-related enzyme: Inhibition of chitinase and mRNA accumulation in cultured tobacco tissues by auxin and cytokinins. Proc. Natl. Acad. Sci. USA 84:89-93.
42. Smith, S. E., and Read, D. J., eds. 1995. Mycorrhizal Symbiosis. Academic Press, NY. pp. 105-160.
43. Spanu, P., Boller, T., Ludwig, A., Wiemken, A., Faccio, A., and Bonfante-Fasolo, P. 1989. Chitinase in roots of mycorrhizal Allium porrum: regulation and localization. Planta 177:447-445.
44. van Loon, L. C. 1985. Pathogenesis-related proteins. Plant Mol. Biol. 4: 111-116.
45. Vernooij, B., Friedrich, L., Ahl Goy, P., Staub, T., Kessmann, H., and Ryals, J. 1995. 2,6-Dichloroisonicotinic acid-induced resistance to pathogens without the accumulation of salicylic acid. Mol. Plant-Microbe Interact. 8:228-234.
46. Vierheilig, H., Alt, M., Lange, J., Gut-Rella, M., Wiemken, A., and Boller, T. 1995. Colonization of transgenic constitutively expressing pathogenesis-related proteins by the vesicular-arbuscular mycorrhizal fungi Glomus mosseae. Appl. Environ. Microbiol. 61:3031-3034.
47. Volpin, H., Phillips, D. A., Okon, Y., and Kapulnik, Y. 1995. Suppression of an isoflavenoid phytoalexin defense response in mycorrhizal alfalfa roots. Plant Physiol. 108:1449-1454.
48. Ward, E. R., Payne, G. B., Moyer, M. B., Williams, S. C., Dincher, S. S., Sharkey, K. C., Beck, J. J., Taylor, H. T., Ahl-Goy, P., Mains, F., and Ryals, J. A. 1991a. Differential regulation of β-1,3-glucanase messenger RNAs in response to pathogen infection. Plant Physiol. 96:390-397.
49. Ward, E. R, Uknes, S. J., Williams, S. C., Dincher, S. S., Wiederhold, D. L., Alexander, D. C., Ahl-Goy, P., Métraux, J.-P., and Ryals, J. 1991b. Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3:1085-1094.
50. Wyatt, S. E., Pan, S. Q., and Kúc, J. 1991. β-1,3-glucanase, chitinase, and peroxidase activity in tobacco tissues resistant and susceptible to blue mold as related to flowering, age and sucker development. Physiol. Mol. Plant Pathol. 39:433-440.
51. Yalpani, N., Silverman, P., Wilson, T. M. A., Kleier, D. A., and Raskin, I. 1991. Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3:809-818.
52. Yoshikawa, M., Tsuda, M., and Takeuchi, Y. 1994. Resistance to fungal disease in transgenic tobacco plants expressing the phytoalexin elicitor-releasing factor, β-1,3-endoglucanase from soybean. Naturwissenschaften 80:417-420.
53. Young, J. K., and Hwang, B. K. 1994. Differential accumulation of β-1,3-glucanase and chitinase isoforms in pepper stem infected by compatible and incompatible isolates of Phytophthora capsici. Physiol. Mol. Plant Pathol. 45:195-209.
54. Zhu, Q., Maher, E. A., Msoud, S., Dixon, R. A., and Lamb, C. J. 1994. Enhanced protection against fungal attack by constitutive co-expression of chitinase and glucanase genes in transgenic tobacco. Biotechnology 12:807-812.