In spite of induced multiple defense responses, tomato plants infected with Cucumber mosaic virus and D satellite RNA succumb to systemic necrosis

Molecular Plant-Microbe Interactions

Volumn 16, Issue 6, 2003, Pages 467-476

  Xu, Ping ^a   Blancaflor, Elison B ^a   Roossinck, Marilyn J ^a  

^a PLANT BIOLOGY DIVISION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; CUCUMBER MOSAIC VIRUS; CUCUMIS SATIVUS; LYCOPERSICON ESCULENTUM; NICOTIANA TABACUM;

EID: 0037572146     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.2003.16.6.467     Document Type: Article

References (57)

1. Anfoka, G., and Buchenauer, H. 1997. Systemic acquired resistance in tomato against Phytophthora infestans by pre-inoculation with tobacco necrosis virus. Physiol. Mol. Plant Pathology 50:85-101.
2. Bantignies, B., Séguin, J., Muzac, I., Dédaldéchamp, F., Gulick, P., and Ibrahim, R. 2000. Direct evidence for ribonucleolytic activity of a PR-10-like protein from white lupin roots. Plant Mol. Biol. 42:871-881.
3. Baudouin, E., Charpenteau, M., Roby, D., Marco, Y., Ranjeva, R., and Ranty, B. 1997. Functional expression of a tobacco gene related to the serine hydrolase family Esterase activity towards short-chain dinitrophenyl acylesters. Eur. J. Biochem. 248:700-706.
4. Bernal, J. J., and García-Arenal, F. 1997. Analysis of the in vitro secondary structure of cucumber mosaic virus satellite RNA. RNA 3:1052-1067.
5. Bethke, P. C., and Jones, R. L. 2001. Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. Plant J. 25:19-29.
6. Breda, C., Sallaud, C., el-Turk, J., Buffard, D., deKosak, I., Esnault, R., and Kondorosi, A. 1996. Defense reactions in Medicago sativa: a gene encoding a class 10 PR protein is expressed in vascular bundles. Mol. Plant-Microbe Interact. 9:713-719.
7. Bucher, G. L., Rarina, C., Heinlein, M., DeSerio, F., Fred Meins, J., and Iglesias, V. A. 2001. Local expression of enzymatically active class I β-1,3-glucanase enhances symptoms of TMV infection in tobacco. Plant J. 28:361-369.
8. Cai, X., Takken, F. L. W., Joosten, M. H. A. J., and Wit, P. J. G. M. D. 2001. Specific recognition of AVR4 and AVR9 results in distinct patterns of hypersensitive cell death in tomato, but similar patterns of defense-related gene expression. Mol. Plant Pathol. 2:77-86.
9. 2 in transgenic tobacco. Proc. Natl. Acad. Sci. U.S.A. 95:5818-5823.
10. Church, G. M., and Gilbert, W. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. U.S.A. 81:1991-1995.
11. Cole, A. B., Király, L., Ross, K., and Schoelz, J. E. 2001. Uncoupling resistance from cell death in the hypersensitive response of Nicotiana species to Cauliflower mosaic virus infection. Mol. Plant-Microbe Interact. 14:31-41.
12. Constabel, C. P., and Brisson, N. 1995. Stigma- and vascular-specific expression of the PR10a gene of potato: a novel pattern of expression of a pathogenesis-related gene. Mol. Plant-Microbe Interact. 8:104-113.
13. Donofrio, N. M., and Delaney, T. 2001. Abnormal callose response phenotype and hypersusceptibility to Peronospora parasitica in defense-compromised Arabidopsis nim1-1 and salicylate hydroxylase-expressing plants. Mol. Plant-Microbe Interact. 14:439-450.
14. Du, H., and Klessing, D. F. 1997. Role for salicylic acid in the activation of defense responses in catalase-deficient transgenic tobacco. Mol. Plant-Microbe Interact. 10:922-925.
15. García-Arenal, F., and Palukaitis, P. 1999. Structure and functional relationships of satellite RNAs of cucumber mosaic virus. Pages 37-63 in: Satellites and Defective Viral RNAs. P. K. Vogt and A. O. Jackson, eds. Springer, Berlin.
16. Grieco, F., Lanave, C., and Gallitelli, D. 1997. Evolutionary dynamics of cucumber mosaic virus satellite RNA during natural epidemics in Italy. Virology 229:166-174.
17. Hammond-Kosack, K. E., and Jones, J. D. G. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8:1773-1791.
18. Iglesias, V. A., and Meins, F., Jr. 2000. Movement of plant viruses is delayed in a β-1,3-glucanase-deficient mutant showing a reduced plasmodesmatal size exclusion limit and enhanced callose deposition. Plant J. 21:157-166.
19. Jabs, T. 1999. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem. Pharmacol. 57:231-345.
20. Jordá, C., Alfaro, A., Aranda, M. A., Moriones, E., and García-Arenal, F. 1992. Epidemic of cucumber mosaic virus plus satellite RNA in tomatoes in eastern Spain. Plant Dis. 76:363-366.
21. Kaper, J. M., and Tousignant, M. E. 1977. Cucumber mosaic virus-associated RNA 5 I. Role of host plant and helper strain in determining amount of associated RNA 5 with virions. Virology 80:186-195.
22. Karpinski, S., Reynolds, H., Karpinski, B., Wingsle, G., Creissen, G., and Mullineaux, P. 1999. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654-657.
23. Kawai-Yamada, M., Jin, L., Yoshinaga, K., Hirata, A., and Uchimiya, H. 2001. Mammalian Bax-induced plant cell death can be down-regulated by overexpression of Arabidopsis Bax Inhibitor-1 (ATBI-1). Proc. Natl. Acad. Sci. U.S.A. 98:12295-12300.
24. Király, L., Cole, A. B., Bourque, J. E., and Schoelz, J. E. 1999. Systemic cell death is elicited by the interaction of a single gene in Nicotiana clevelandii and gene VI of Cauliflower mosaic virus. Mol. Plant-Microbe Interact. 12:919-925.
25. Koiwa, H., Kato, H., Nakatsu, T., Oda, J., Yamada, Y., and Sato, F. 1997. Purification and characterization of tobacco pathogenesis-related proteins PR-5d, an antifungal thaumatin-like protein. Plant Cell Physiol. 38:783-791.
26. Lam, E., Kato, N., and Lawton, M. 2001. Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411:848-853.
27. Lamb, C., and Dixon, R. A. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:251-275.
28. Matton, D. P., and Brisson, N. 1989. Cloning, expression, and sequence conservation of pathogenesis-related gene transcripts of potato. Mol. Plant-Microbe Interact. 2:325-331.
29. McGee, J. D., Hamer, J. E., and Hodges, T. K. 2001. Characterization of a PR-10 Pathogenesis-related gene family induced in rice during infection with Magnaporthe grisea. Mol. Plant-Microbe Interact. 14:877-886.
30. Mittler, R., Herr, E. H., Orvar, B. L., vanCamp, W., Willekens, H., Inzé, D., and Ellis, B. E. 1999. Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc. Natl. Acad. Sci. U.S.A. 96:14165-14170.
31. Moiseyev, G. P., Beintema, J. J., Fedoreyeva, L. I., and Yakovlev, G. I. 1994. High sequence similarity between a ribonuclease from ginseng calluses and fungus-elicited proteins from parsley indicates that intracellular pathogenesis-related proteins are ribonucleases. Planta 193:470-472.
32. Niderman, T., Genetet, I., Bruyère, T., Gees, R., Stintzi, A., Legrand, M., Fritig, B., and Mösinger, E. 1995. Pathogenesis-related PR-1 proteins are antifungal. Plant Physiol. 108:17-27.
33. Orozco-Cárdenas, M. L., Narváez-Vásquez, J., and Ryan, C. A. 2001. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl janmonate. Plant Cell 13:179-191.
34. Palukaitis, P., Roossinck, M. J., Dietzgen, R. G., and Francki, R. I. B. 1992. Cucumber mosaic virus. Pages 281-348 in: Advances in Virus Research. K. Maramorosch, F. A. Murphy, and A. J. Shatkin, eds. Academic Press, San Diego, CA, U.S.A.
35. Pontier, D., Godiard, L., Marco, Y., and Roby, D. 1994. hsr203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant/pathogen interactions. Plant J. 5:507-521.
36. Rodríguez-Alvarado, G., and Roossinck, M. J. 1997. Structural analysis of a necrogenic strain of cucumber mosaic cucumovirus satellite RNA in planta. Virology 236:155-166.
37. Roossinck, M. J., and White, P. S. 1998. Cucumovirus isolation and RNA extraction. Pages 189-196 in: Plant Virology Protocols. G. D. Foster and S. C. Taylor, eds. Humana Press, Totowa, NJ, U.S.A.
38. Sanchez, P., Zabala, M. D., and Grant, M. 2000. AtBI-1, a plant homologue of Bax Inhibitor-1, suppresses Bax-induced cell death in yeast and is rapidly upregulated during wounding and pathogen challenge. Plant J. 21:393-399.
39. Scandalios, J. G. 1994. Regulation and properties of plant catalases. In: Cause of Photoxidative Stress and Amelioration of Defense Systems in Plants. C. H. Foyer and P. M. Mullineaux, eds. CRC Press. Boca Raton, FL, U.S.A.
40. Schmelzer, E., Krüger-Lebus, S., and Hahlbrock, C. 1989. Temporal and spatial patterns of gene expression around sites of attempted fungal infection in parsley leaves. Plant Cell 1:993-1001.
41. Sleat, D. E., and Palukaitis, P. 1990. Site-directed mutagenesis of a plant viral satellite RNA changes its phenotype from ameliorative to necrogenic. Proc. Natl. Acad. Sci. U.S.A. 87:2946-2950.
42. Sleat, D. E., Zhang, L., and Palukaitis, P. 1994. Mapping determinants within cucumber mosaic virus and its satellite RNA for the induction of necrosis in tomato plants. Mol. Plant-Microbe Interact. 7:189-195.
43. Smith, M. M., and McCully, M. E. 1978. Enhancing aniline blue fluorescent staining of cell wall structures. Stain Technol. 53:79-85.
44. Sticher, L., Mauch-Mani, B., and Métraux, J. P. 1997. Systemic acquired resistance. Pages 235-270 in: Annual Review of Phytopathology. R. K. Webster, G. Shaner, and N. K. VanAlfen, eds. Annual Reviews Inc., Palo Alto, CA, U.S.A.
45. Takahashi, H., Chen, Z., Du, H., Liu, Y., and Klessig, D. F. 1997. Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels. Plant J. 11:993-1005.
46. Takeda, S., Sato, F., Ida, K., and Yamada, Y. 1991. Nucleotide sequence of a cDNA for osmotin-like protein from cultured tobacco cells. Plant Physiol. 97:844-846.
47. Taliansky, M. E., Ryabov, E. V., Robinson, D. J., and Palukaitis, P. 1998. Tomato cell death mediated by complementary plant viral satellite RNA sequences. Mol. Plant-Microbe Interact. 11:1214-1222.
48. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11:1187-1194.
49. Tornero, P., Conejero, V., and Vera, P. 1994. A gene encoding a novel isoform of the PR-1 protein family from tomato is induced upon viroid infection. Mol. Gen. Genet. 243:47-53.
50. Tornero, P., Gadea, J., Conejero, V., and Vera, P. 1997. Two PR-1 genes from tomato are differentially regulated and reveal a novel mode of expression for a pathogenesis-related gene during the hypersensitive response and development. Mol. Plant-Microbe Interact. 10:624-634.
51. Tornero, P., Rodrigo, I., Conejero, V., and Vera, P. 1993. Nucleotide sequence of a cDNA encoding a pathogenesis-related protein, P1-p14, from tomato (Lycopersicon esculentum). Plant Physiol. 102:325.
52. Tronchet, M., Ranty, B., Marco, Y., and Roby, D. 2001. HSR203 antisense suppression in tobacco accelerates development of hypersensitive cell death. Plant J. 27:115-127.
53. vanKan, J. A. L., Joosten, M. H. A. J., Wagemakers, C. A. M., vandenBerg-Velthuis, G. C. M., and deWit, P. J. G. M. 1992. Differential accumulation of mRNAs encoding extracellular and intracellular PR proteins in tomato induced by virulent and avirulent races of Cladosporium fulvum. Plant Mol. Biol. 20:513-527.
54. vanLoon, L. C. 1999. Occurrence and properties of plant pathogenesis-related proteins. Pages 1-47 in: Pathogenesis-Related Proteins in Plants. S. K. Datta and S. Muthukrishnan, eds. CRC Press, Boca Raton, FL, U.S.A.
55. Warner, S. A. J., Scott, R., and Draper, J. 1993. Isolation of an asparagus intracellular PR gene (AoPR1) wound-responsive promoter by the inverse polymerase chain reaction and its characterization in transgenic tobacco. Plant J. 3:191-201.
56. Wu, G., and Shah, D. M. 1995. Isolation and characterization of a potato catalase cDNA (GenBank U27082). Plant Gene Register PGR95-037.
57. Xu, P., and Roossinck, M. J. 2000. Cucumber mosaic virus D satellite RNA-induced programmed cell death in tomato. Plant Cell 12:1079-1092.