The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Genetic Stability of Magnaporthe oryzae during Successive Passages through Rice Plants and on Artificial Medium

  • Park, Sook-Young (Department of Agricultural Biotechnology, Center for Fungal Genetic Resources, and Center for Fungal Pathogenesis, Seoul National University) ;
  • Chi, Myoung-Hwan (Department of Agricultural Biotechnology, Center for Fungal Genetic Resources, and Center for Fungal Pathogenesis, Seoul National University) ;
  • Milgroom, Michael G. (Department of Plant Pathology and Plant-Microbe Biology, Cornell University) ;
  • Kim, Hyo-Jung (Department of Agricultural Biotechnology, Center for Fungal Genetic Resources, and Center for Fungal Pathogenesis, Seoul National University) ;
  • Han, Seong-Sook (Agricultural Microbiology Team, National Academy of Agricultural Science, RDA) ;
  • Kang, Seog-Chan (Department of Plant Pathology, The Pennsylvania State University) ;
  • Lee, Yong-Hwan (Department of Agricultural Biotechnology, Center for Fungal Genetic Resources, and Center for Fungal Pathogenesis, Seoul National University)
  • Received : 2010.09.27
  • Accepted : 2010.11.02
  • Published : 2010.12.01
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Abstract

Genetic instability of the rice blast fungus Magnaporthe oryzae has been suggested as a major factor underlying the rapid breakdown of host resistance in the field. However, little information is available on the mechanism of genetic instability. In this study, we assessed the stability of repetitive DNA elements and several key phenotypic traits important for pathogenesis after serially transferring two isolates though rice plants and an artificial medium. Using isolate 70-15, we obtained a total of 176 single-spore isolates from 10 successive rounds of culturing on artificial medium. Another 20 isolates were obtained from germ tubes formed at the basal and apical cells of 10 three-celled conidia. Additionally, 60 isolates were obtained from isolate KJ201 after serial transfers through rice plants and an artificial medium. No apparent differences in phenotypes, including mycelial growth, conidial morphologies, conidiation, conidial germination, appressorium formation, and virulence, or in DNA fingerprints using MGR586, MAGGY, Pot2, LINE, MG-SINE and PWL2 as probes were observed among isolates from the same parent isolate. Southern hybridization and sequence analysis of two avirulence genes, AVR-Pita1 and AVR-Pikm, showed that both genes were also maintained stably during 10 successive generations on medium and plants. However, one reversible loss of restriction fragments was found in the telomere-linked helicase gene (TLH1) family, suggesting some telomere regions may be more unstable than the rest of the genome. Taken together, our results suggest that phenotype and genotype of M. oryzae isolates do not noticeably change, at least up to 10 successive generations on a cultural medium and in host plants.

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References

  1. Bonman, J. M., Vergel de Dois, T. I. and Khin, M. M. 1986. Physiologic specialization of Pyricularia oryzae in the Philippines. Plant Dis. 70:767-769. https://doi.org/10.1094/PD-70-767
  2. Borromeo, E. S., Nelson, R. J., Bonman, J. M. and Leung, H. 1993. Genetic differentiation among isolates of Pyricularia infecting rice and weed hosts. Phytopathology 83:393-399. https://doi.org/10.1094/Phyto-83-393
  3. Chen, D., Zeigler, R. S., Leung, H. and Nelson, R. J. 1995. Population structure of Pyricularia grisea at two screening sites in the Philippines. Phytopathology 85:1011-1020. https://doi.org/10.1094/Phyto-85-1011
  4. Chi, M. H., Park, S. Y., Kim, S. and Lee, Y. H. 2009. A novel pathogenicity gene is required in the rice blast fungus to suppress the basal defenses of the host. PLoS Pathog. 5:e1000401. https://doi.org/10.1371/journal.ppat.1000401
  5. Correa-Victoria, F. J. and Zeigler, R. S. 1993. Field breeding for durable rice blast resistance in the presence of diverse pathogen populations. Edited by Jacobs, T & Parleviet, JR, Durability of Disease Resistance. Norwell: Kluwer Academic Publishers.
  6. Correa-Victoria, F. K. and Zeigler, R. S. 1993. Pathogenic variability in Pyricularia grisea at a rice blast “hot spot” breeding site in eastern Colombia. Plant Dis. 77:1029-1035. https://doi.org/10.1094/PD-77-1029
  7. Dean, R. A., Talbot, N. J., Ebbole, D. J. Farman, M. L., Mitchell, T. K., Orbach, M. J., Thon, M., Kulkarni, R., Xu, J. R., Pan, H., Read, N. D., Lee, Y. H., Carbone, I., Brown, D., Oh, Y. Y., Donofrio, N., Jeong, J. S., Soanes, D. M., Djonovic, S., Kolomiets, E., Rehmeyer, C., Li, W., Harding, M., Kim, S., Lebrun, M. H., Bohnert, H., Coughlan, S., Butler, J., Calvo, S., Ma, L. J., Nicol, R., Purcell, S., Nusbaum, C., Galagan, J. E., and Birren, B. W. 2005. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434:980-986. https://doi.org/10.1038/nature03449
  8. Feng, S., Ma, J., Lin, F., Wang, L. and Pan, Q. 2007. Construction of an electronic physical map of Magnaporthe oryzae using genomic position-ready SSR markers. Chin. Sci. Bull. 52: 3346-3354. https://doi.org/10.1007/s11434-007-0498-0
  9. Gao, W., Khang, C. H., Park, S.-Y., Lee, Y.-H. and Kang, S. 2002. Evolution and organization of a highly dynamic, subtelomeric helicase gene family in the rice blast fungus Magnaporthe grisea. Genetics 162:103-112.
  10. Genovesi, A. D. and Magill, C. W. 1976. Heterokaryosis and parasexuality in Pyricularia oryzae Cavara. Can. J. Microbiol. 22:531-536. https://doi.org/10.1139/m76-079
  11. Han, S. S., Ra, D. S., Choi, S. H. and Kim, C. K. 1997. Population dynamics of Pyricularia grisea during leaf and panicle blast stages in the same field. Korean J. Plant Pathol. 13:408-415.
  12. Jeon, J., Goh, J., Yoo, S., Chi, M. H., Choi, J., Rho, H. S., Park, J., Han, S. S., Kim, B. R., Park, S. Y., Kim, S., and Lee, Y. H. 2008. A putative MAP kinase kinase kinase, MCK1, is required for cell wall integrity and pathogenicity of the rice blast fungus, Magnaporthe oryzae. Mol. Plant-Microbe. Interact. 21:525-534. https://doi.org/10.1094/MPMI-21-5-0525
  13. Jeon, J., Park, S. Y., Chi, M. H., Choi, J., Park, J., Rho, H. S., Kim, S., Goh, J., Yoo, S., Park, J. Y., Yi, M., Yang, S., Kwon, M. J., Han, S. S., Kim, B. R., Khang, C. H., Park, B., Lim, S. E., Jung, K., Kong, S., Karunakaran, M., Oh, H. S., Kim, H., Kang, S., Choi, W. B., and Lee, Y. H. 2007. Genome-wide functional analysis of pathogenicity genes in the rice blast fungus. Nat. Genet. 39:561-565. https://doi.org/10.1038/ng2002
  14. Kachroo, P., Leong, S. A. and Chattoo, B. B. 1994. Pot2, an inverted repeat transposon from the rice blast fungus Magnaporthe grisea. Mol. Gen. Genet. 245:339-348. https://doi.org/10.1007/BF00290114
  15. Kachroo, P., Leong, S. A. and Chattoo, B. B. 1995. Mg-SINE: a short interspersed nuclear element from the rice blast fungus, Magnaporthe grisea. Proc. Natl. Acad. Sci. USA 92:11125-11129. https://doi.org/10.1073/pnas.92.24.11125
  16. Kang, S. and Lee, Y.-H. 2000. Population structure and race variation of the rice blast fungus. Plant Pathol. J. 16:1-8.
  17. Kang, S., Lebrun, M.-H., Farrall, L. and Valent, B. 2001. Gain of virulence caused by insertion of a Pot3 transposon in a Magnaporthe grisea avirulence gene. Mol. Plant- Microbe Interact. 14:671-674. https://doi.org/10.1094/MPMI.2001.14.5.671
  18. Khang, C. H., Park, S. Y., Lee, Y. H., Valent, B. and Kang, S. 2008. Genome organization and evolution of the AVR-Pita avirulence gene family in the Magnaporthe grisea species complex. Mol. Plant-Microbe Interact. 21:658-670. https://doi.org/10.1094/MPMI-21-5-0658
  19. Latterell, F. M. and Rossi, A. E. 1986. Longevity and pathogenic stability of Pyricularia oryzae. Phytopathology 76:231-235. https://doi.org/10.1094/Phyto-76-231
  20. Levy, M., Correa-Victoria, F. J., Zeigler, R. S., Hu, S. and Hamer, J. E. 1993. Genetic diversity of the rice blast fungus in a disease nursery in Colombia. Phytopathology 83:1427-1433. https://doi.org/10.1094/Phyto-83-1427
  21. Nishimura, M., Hayashi, N., Jwa, N. S., Lau, G. W., Hamer, J. E. and Hasebe, A. 2000. Insertion of the LINE retrotransposon MGL causes a conidiophore pattern mutation in Magnaporthe grisea. Mol. Plant Microbe-Interact. 13:892-894. https://doi.org/10.1094/MPMI.2000.13.8.892
  22. Noguchi, M. T., Yasuda, N. and Fujita, Y. 2006. Evidence of genetic exchange by parasexual recombination and genetic analysis of pathogenicity and mating type of parasexual recombinants in rice blast fungus. Magnaporthe oryzae. Phytopathology 96:746-750. https://doi.org/10.1094/PHYTO-96-0746
  23. Orbach, M. J., Farrall, L., Sweigard, J. A., Chumley, F. G. and Valent, B. 2000. A telomeric avirulence gene determines efficacy for rice blast resistance gene Pi-ta. Plant Cell 12:2019-2032. https://doi.org/10.1105/tpc.12.11.2019
  24. Park, S.-Y., Jwa, N. S., Chi, M.-H. and Lee, Y.-H. 2009. A fluorescence-based cDNA-AFLP method for identification of differentially expressed genes. Plant Pathol. J. 25:184-188. https://doi.org/10.5423/PPJ.2009.25.2.184
  25. Park, S.-Y., Milgroom, M. G., Han, S. S., Kang, S. and Lee, Y.-H. 2003. Diversity of pathotypes and DNA fingerprint haplotypes in populations of Magnaporthe grisea in Korea over two decades. Phytopathology 93:1378-1385. https://doi.org/10.1094/PHYTO.2003.93.11.1378
  26. Rao, K. M. 1994. Rice blast disease. Delhi-119935: Daya publishing house.
  27. Sweigard, J. A., Carroll, A. M., Kang, S., Farrall, L., Chumley, F. G. and Valent, B. 1995. Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. Plant Cell 7:1221-1233. https://doi.org/10.1105/tpc.7.8.1221
  28. Valent, B., Farrall, L., and Chumley, F. G. 1991. Magnaporthe grisea genes for pathogenicity and virulence identified through a series of backcrosses. Genetics 127:87-101.
  29. Wu, B. C. and Magill, C. W. 1995. Spontaneous mutations at fingerprint loci in clonal lineages of the rice blast fungus. Exp. Mycol. 19:86-90. https://doi.org/10.1006/emyc.1995.1010
  30. Xia, J. Q. and Correll, J. C. 1995. Examination of mitotic stability and hybridization potential between two genetically distinct haplotypes of Magnaporthe grisea. Exp. Mycol. 19:171-177. https://doi.org/10.1006/emyc.1995.1021
  31. Xia, J. Q., Correll, J. C., Lee, F. N. and Ross, W. J. 2000. Regional population diversity of Pyricularia grisea in Arkansas and the influence of host selection. Plant Dis. 84:877-884. https://doi.org/10.1094/PDIS.2000.84.8.877
  32. Xia, J. Q., Correll, J. C., Lee, F. N., Marchetti, M. A. and Rhoads, D. D. 1993. DNA fingerprinting to examine microgeographic variation in the Magnaporthe grisea (Pyricularia grisea) population in two rice fields in Arkansas. Phytopathology 83: 1029-1035. https://doi.org/10.1094/Phyto-83-1029
  33. Zeigler, R. S., Scott, R. P., Leung, H., Bordeos, A. A., Kumar, J. and Nelson, R. J. 1997. Evidence of parasexual exchange of DNA in the rice blast fungus challenges its exclusive clonality. Phytopathology 87:284-294. https://doi.org/10.1094/PHYTO.1997.87.3.284
  34. Zhou, E., Jia, Y., Singh, P., Correll, J. and Lee, F. N. 2007. Instability of the Magnaporthe oryzae avirulence gene AVR-Pita alters virulence. Fungal Genet. Biol. 44:1024-1034. https://doi.org/10.1016/j.fgb.2007.02.003

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