An avirulent tomato powdery mildew isolate induces localized acquired resistance to a virulent isolate in a spatiotemporal manner

Molecular Plant-Microbe Interactions

Volumn 25, Issue 3, 2012, Pages 372-378

  Seifi, Alireza ^a   Nonomura, Teruo ^b   Matsuda, Yoshinori ^b   Toyoda, Hideyoshi ^b   Bai, Yuling ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b KINKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PLANT DNA; RIBOSOMAL SPACER DNA; VEGETABLE PROTEIN;

ARTICLE; ASCOMYCETES; CELL DEATH; CHEMISTRY; DISEASE RESISTANCE; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYLOGENY; PHYSIOLOGY; PLANT DISEASE; PLANT EPIDERMIS; TOMATO; TRANSGENIC PLANT;

ASCOMYCOTA; BASE SEQUENCE; CELL DEATH; DISEASE RESISTANCE; DNA, PLANT; DNA, RIBOSOMAL SPACER; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; PLANT EPIDERMIS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SEQUENCE ANALYSIS, DNA;

ERYSIPHALES; LYCOPERSICON ESCULENTUM;

EID: 84857577889     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-06-11-0171     Document Type: Article

References (38)

1. Bai, Y., van der Hulst, R., Bonnema, G., Marcel, T., Meijer-Dekens, F., Niks, R., and Lindhout, P. 2005. Tomato defense to Oidium neolycopersici: Dominant Ol genes confer isolate-dependent resistance via a different mechanism than recessive ol-2. Mol. Plant-Microbe Interact. 18:354-362. (Pubitemid 40383903)
2. Bai, Y. L., Huang, C. C., van der Hulst, R., Meijer-Dekens, F., Bonnema, G., and Lindhout, P. 2003. QTLs for tomato powdery mildew resistance (Oidium lycopersici) in Lycopersicon parviflorum G1.1601 co-localize with two qualitative powdery mildew resistance genes. Mol. Plant-Microbe Interact. 16:169-176. (Pubitemid 36128699)
3. Cordelier, S., de Ruffray, P., Fritig, B., and Kauffmann, S. 2003. Biological and molecular comparison between localized and systemic acquired resistance induced in tobacco by a Phytophthora megasperma glycoprotein elicitin. Plant Mol. Biol. 51:109-118. (Pubitemid 36189139)
4. Costet, L., Cordelier, S., Dorey, S., Baillieul, F., Fritig, B., and Kauffmann, S. 1999. Relationship between localized acquired resistance (LAR) and the hypersensitive response (HR): HR is necessary for LAR to occur and salicylic acid is not sufficient to trigger LAR. Mol. Plant-Microbe Interact. 12:655-662. (Pubitemid 29355147)
5. Cui, J., Bahrami, A. K., Pringle, E. G., Hernandez-Guzman, G., Bender, C. L., Pierce, N. E., and Ausubel, F. M. 2005. Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc. Natl. Acad. Sci. U.S.A.102:1791-1796. (Pubitemid 40209246)
6. Dixon, R. A. 2001. Natural products and plant disease resistance. Nature 411:843-847. (Pubitemid 32588112)
7. Durrant, W. E., and Dong, X. 2004. Systemic acquired resistance. Annu. Rev. Phytopathol. 42:185-209. (Pubitemid 39308511)
8. Felsenstein, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783-791.
9. Fujita, K., Matsuda, Y., Wada, M., Hirai, Y., Mori, K., Moriura, N., Nonomura, T., Kakutani, K., and Toyoda, H. 2004. Powdery mildew pathogens can suppress the chitinase gene expression induced in detached inner epidermis of barley coleoptile. Plant Cell Rep. 23:504-511. (Pubitemid 40047543)
10. Gardes, M., and Bruns, T. D. 1993. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol. Ecol. 2:113-118.
11. Hammerschmidt, R. 2009. Systemic acquired resistance. Adv. Bot. Res. 51:173-222.
12. Holdaway-Clarke, T. L., Walker, N. A., Hepler, P. K., and Overall, R. L. 2000. Physiological elevations in cytoplasmic free calcium by cold or ion injection result in transient closure of higher plant plasmodesmata. Planta 210:329-335. (Pubitemid 30067898)
13. Huang, C. C., Groot, T., Meijer-Dekens, F., Niks, R. E., and Lindhout, P. 1998. The resistance to powdery mildew (Oidium lycopersicum) in Lycopersicon species is mainly associated with hypersensitive response. Eur. J. Plant Pathol. 104:399-407. (Pubitemid 28333003)
14. Huang, C. C., Hoefs-van de Putte, P. M., Haanstra-van der Meer, J. G., Meijer-Dekens, F., and Lindhout, P. 2000. Characterization and mapping of resistance to Oidium lycopersicum in two Lycopersicon hirsutum accessions: Evidence for close linkage of two Ol-genes on chromosome 6 of tomato. Heredity 85:511-520. (Pubitemid 32200609)
15. Hughes, J., and Gunning, B. 1980. Glutaraldehyde-induced deposition of callose. Can. J. Bot. 58:250-258.
16. Ivic, D., Milicevic, T., and Cvjetkovic, B. 2009. First Croatian report of powdery mildew on tomato caused by Oidium neolycopersici. Plant Pathol. 58:802-802.
17. Jones, H., Whipps, J. M., and Gurr, S. J. 2001. The tomato powdery mildew fungus Oidium neolycopersici. Mol. Plant Pathol. 2:303-309. (Pubitemid 34025609)
18. Kashimoto, K., Sameshima, T., Matsuda, Y., Nonomura, T., Oichi, W., Kakutani, K., Nakata, K., Kusakari, S., and Toyoda, H. 2003. Infectivity of a Japanese isolate of Oidium neolycopersici KTP-01 to a European tomato cultivar resistant to O. lycopersici. J. Gen. Plant Pathol. 69:406-408.
19. Kiss, L., Cook, R. T. A., Saenz, G. S., Cunnington, J. H., Takamatsu, S., Pascoe, I., Bardin, M., Nicot, P. C., Sato, Y., and Rossman, A. Y. 2001. Identification of two powdery mildew fungi, Oidium neolycopersici sp. nov. and O. lycopersici, infecting tomato in different parts of the world. Mycol. Res. 105:684-697. (Pubitemid 32643806)
20. Li, C. W., Bonnema, G., Che, D., Dong, L., Lindhout, P., Visser, R., and Bai, Y. L. 2007. Biochemical and molecular mechanisms involved in monogenic resistance responses to tomato powdery mildew. Mol. Plant-Microbe Interact. 20:1161-1172. (Pubitemid 47281782)
21. Love, A., Milner, J., and Sadanandom, A. 2008. Timing is everything: Regulatory overlap in plant cell death. Trends Plant Sci. 13:589-595.
22. Matsuda, Y., Mori, Y., Sakano, Y., Nishida, M., Tarumoto, K., Nonomura, T., Nishimura, H., Kusakari, S., and Toyoda, H. 2005. Screening of wild Lycopersicon species for resistance to Japanese isolate of tomato powdery mildew Oidium neolycopersici. Breed. Sci. 55:355-360. (Pubitemid 41390124)
23. Matsuda, Y., Ikeda, H., Moriura, N., Tanaka, N., Shimizu, K., Oichi, W., Nonomura, T., Kakutani, K., Kusakari, S., Higashi, K., and Toyoda, H. 2006. A new spore precipitator with polarized dielectric insulators for physical control of tomato powdery mildew. Phytopathology 96:967-974. (Pubitemid 44300198)
24. Nimchuk, Z., Eulgem, T., Holt Iii, B. F., and Dangl, J. L. 2003. Recognition and response in the plant immune system. Annu. Rev. Genet. 37:579-609. (Pubitemid 38041438)
25. Nonomura, T., Matsuda, Y., Xu, L., Kakutani, K., Takikawa, Y., and Toyoda, H. 2009. Collection of highly germinative pseudochain conidia of Oidium neolycopersici from conidiophores by electrostatic attraction. Mycol. Res. 113:364-372.
26. Nonomura, T., Nishitomi, A., Matsuda, Y., Soma, C., Xu, L., Kakutani, K., Takikawa, Y., and Toyoda, H. 2010. Polymorphic change of appressoria by the tomato powdery mildew Odium neolycopersici on host tomato leaves reflects multiple unsuccessful penetration attempts. Fungal Biol. 114:917-928.
27. Parker J. E. 2009. The quest for long-distance signals in plant systemic immunity. Sci. Signal. 2:1-3.
28. Ross, A. F. 1961a. Localized acquired resistance to plant virus infection in hypersensitive hosts. Virology 14:329-339.
29. Ross, A. F. 1961b. Systemic acquired resistance induced by localized virus infections in plants. Virology 14:340-358.
30. Ryals, J., Uknes, S., and Ward, E. 1994. Systemic acquired resistance. Plant Physiol. 104:1109-1112.
31. Sameshima, T., Kashimoto, K., Kida, K., Matsuda, Y., Nonomura, T., Kakutani, K., Nakata, K., Kusakari, S., and Toyoda, H. 2004. Cytological events in tomato leaves inoculated with conidia of Blumeria graminis f. sp. hordei and Oidium neolycopersici KTP-01. J. Gen. Plant Pathol. 70:7-10. (Pubitemid 38871699)
32. Seifi, A. 2011. Characterization of tomato genes for resistance to Oidium neolycopersici. Ph.D. thesis, Wageningen University, Wageningen, Wageningen, The Netherlands.
33. Seifi, A., Kaloshian, I., Vossen, J., Che, D. D., Bhattarai, K. K., Fan, J. M., Naher, Z., Goverse, A., Tjallingii, W. F., Lindhout, P., Visser, R. G. F., and Bai, Y. L. 2011. Linked, if not the same, Mi-1 homologues confer resistance to tomato powdery mildew and root-knot nematodes. Mol. Plant-Microbe Interact. 24:441-450.
34. Szentiványi, O., Kiss, L., Russell, J. C., Kovács, G. M., Varga, K., Jankovics, T., Lesemann, S., Xu, X.-M., and Jeffries, P. 2005. Ampelomyces mycoparasites from apple powdery mildew identified as a distinct group based on single-stranded conformation polymorphism analysis of the rDNA ITS region. Mycol. Res. 109:429-438. (Pubitemid 40623429)
35. Tucker, E. B., and Boss, W. F. 1996. Mastoparan-induced intracellular Ca2+ fluxes may regulate cell-to-cell communication in plants. Plant Physiol. 111:459-467. (Pubitemid 126640490)
36. White, T. J., Bruns, T., Lee, S., and Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Pages 315-322 in: PCR Protocols: A Guide to Methods and Applications. M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White, eds. Academic Press, San Diego, CA, U.S.A
37. Yarwood, C. E. 1960. Localized acquired resistance to tobacco mosaic virus. Phytopathology 50:741-744.
38. Yolageldi, L., Sin, B., and Onogur, E. 2008. First report of Oidium neolycopersici on tomatoes in Turkey. Plant Pathol. 57:373-373.