Research in Plant Disease (식물병연구)

The Korean Society of Plant Pathology (한국식물병리학회)
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Avirulence Gene AVR-Pita1 in the Rice Blast Fungus

벼도열병균의 비병원성 유전자 AVR-Pita1

  • Park, Sook-Young (Department of Plant Medicine, College of Life Science and Natural Resources, Sunchon National University)
  • 박숙영 (순천대학교 식물의학과)
  • Received : 2019.03.12
  • Accepted : 2019.03.22
  • Published : 2019.03.31
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Abstract

The rice blast fungus, Magnaporthe oryzae, is one of the most economically important crop diseases. In addition, rice-M. oryzae interaction is a classical gene-for-gene host-pathogen system. Race variation in pathogen groups was proposed as the main mechanism for rapid break-down of resistance in newly introduced rice cultivars. These new pathogen race variations may be caused by changes in an avirulence gene, such as (i) point mutations, (ii) insertion of transposons, and (iii) frame shifts. The avirulence gene AVR-Pita1 is representative avirulence gene in which all of these mutations are reported. In this review, we present a useful information for avirulence gene AVR-Pita1 and its homologous genes AVR-Pita2 and AVR-Pita3. We also review examples that cause mutations in these evolutionarily significant genes.

벼도열병균은 벼를 재배하는 모든 지역에서 경제적으로 매우 중요한 병이다. 또한, 벼도열병균은 기주인 벼와 유전자 대유전자설이 적용되는 대표적인 식물병원균 모델이다. 재배지에 도입된 새로운 저항성 벼 품종의 빠른 저항성 상실은 병원균 집단의 레이스 변이가 주요 메커니즘으로 제안되고 있다. 이러한 새로운 레이스 변이는 저항성 유전자에 대항하는 비병원성 유전자의 변이에 의해 나타날 수 있는데, (i) 점돌연변이, (ii) 전이인자(transposon)의 삽입, (iii) frame shift등이 그 대표적인 예라고 할 수 있다. 비병원성 유전자 AVR-Pita1은 이러한 다양한 변이의 원인들이 모두 보고된 대표적인 비병원성 유전자이다. 이 총설에서는 비병원성 유전자 AVR-Pita1에 관한 다양한 정보를 제시하고, 상동성 유전자들인 AVR-Pita2 및 AVR-Pita3 유전자를 정리하였다. 이와 함께, 변이의 원인이 되는 다양한 예제를 리뷰 하였다.

Keywords

References

  1. Bent, A. F. 1996. Plant disease resistance genes: function meets structure. Plant Cell 8: 1757-1771. https://doi.org/10.1105/tpc.8.10.1757
  2. Bonman, J. M., Vergel De Dios, T. I., Bandong, J. M. and Lee, E. J. 1987. Pathogenic variability of monoconidial isolates of Pyricularia oryzae in Korea and in the Philippines. Plant Dis. 71: 127-130. https://doi.org/10.1094/PD-71-0127
  3. Bonman, J. M., Khush, G. S. and Nelson, R. J. 1992. Breeding rice for resistance to pests. Annu. Rev. Phytopathol. 30: 507-528. https://doi.org/10.1146/annurev.py.30.090192.002451
  4. Bryan, G. T., Wu, K.-S., Farrall, L., Jia, Y., Hershey, H. P., McAdams, S. A. et al. 2000. A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pita. Plant Cell 12: 2033-2046. https://doi.org/10.1105/tpc.12.11.2033
  5. Carlson, M., Celenza, J. L. and Eng, F. J. 1985. Evolution of the dispersed SUC gene family of Saccharomyces by rearrangements of chromosome telomeres. Mol. Cell. Biol. 5: 2894-2902. https://doi.org/10.1128/MCB.5.11.2894
  6. Charron, M. J. and Michels, C. A. 1988. The naturally occurring alleles of MAL1 in Saccharomyces species evolved by various mutagenic processes including chromosomal rearrangement. Genetics 120: 83-93. https://doi.org/10.1093/genetics/120.1.83
  7. 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
  8. Chen, Q. H., Wang, Y. C. and Zheng, X. B. 2006. Genetic diversity of Magnaporthe grisea in China as revealed by DNA fingerprinting haplotypes and pathotypes. J. Phytopathol. 154: 361-369. https://doi.org/10.1111/j.1439-0434.2006.01106.x
  9. Chuma, I., Isobe, C., Hotta, Y., Ibaragi, K., Futamata, N., Kusaba, M. et al. 2011. Multiple translocation of the AVR-Pita effector gene among chromosomes of the rice blast fungus Magnaporthe oryzae and related species. PLoS Pathog. 7: e1002147. https://doi.org/10.1371/journal.ppat.1002147
  10. Correa-Victoria, F. J. and Zeigler, R. S. 1991. Stable resistance and pathogenic variability in the rice Pyricularia oryzae complex. In: Rice in Latin America: Improvement, management, marketing, ed. by F. Cuevas-Perez, pp. 240. CIAT, Cali, Colombia.
  11. Correa-Victoria, F. J., Zeigler, R. S. and Levy, M. 1994. Virulence characteristics of genetic families of Pyricularia grisea in Columbia. In: Rice blast disease, eds. by R. S. Zeigler, S. A. Leong, and P. S. Teng, pp. 211-229. CAB international, Wallingford, UK.
  12. Correll, J. C., Harp, T. L., Guerber, J. C., Zeigler, R. S., Liu, B., Cartwright, R. D. et al. 2000. Characterization of Pyricularia grisea in the United States using independent genetic and molecular markers. Phytopathology 90: 1396-1404. https://doi.org/10.1094/PHYTO.2000.90.12.1396
  13. Cutt, J. R. and Klessig, D. F. 1992. Pathogenesis-related proteins. In: Genes involved in plant defense, eds. by T. Boller and F. Meins, pp. 209-243. Spring-Verlag, New York, NY, USA.
  14. Dai, Y., Winston, E., Correll, J. C. and Jia, Y. 2014. Induction of avirulence by AVR-Pita1 in virulent U.S. field isolates of Magnaporthe oryzae. Crop J. 2: 1-9. https://doi.org/10.1016/j.cj.2013.12.002
  15. Deng, Y., Zhai, K., Xie, Z., Yang, D., Zhu, X., Liu, J. et al. 2017. Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 355: 962-965. https://doi.org/10.1126/science.aai8898
  16. Don, L. D., Kusaba, M., Urashima, A. S., Tosa, Y., Nakayashiki, H. and Mayama, S. 1999. Population structure of the rice blast fungus in Japan examined by DNA fingerprinting. Ann. Phytopathol. Soc. Jpn. 65: 15-24. https://doi.org/10.3186/jjphytopath.65.15
  17. Farman, M. L., Tosa, Y., Nitta, N. and Leong, S. A. 1996a. MAGGY, a retrotransposon in the genome of the rice blast fungus Magnaporthe grisea. Mol. Gen. Genet. 251: 665-674.
  18. Farman, M. L., Taura, S. and Leong, S. A. 1996b. The Magnaporthe grisea DNA fingerprinting probe MGR586 contains the 3' end of an inverted repeat transposon. Mol. Gen. Genet. 251: 675-681.
  19. Flor, H. H. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9: 275-296. https://doi.org/10.1146/annurev.py.09.090171.001423
  20. Fukuoka, S., Yamamoto, S.-I., Mizobuchi, R., Yamanouchi, U., Ono, K., Kitazawa, N. et al. 2014. Multiple functional polymorphisms in a single disease resistance gene in rice enhance durable resistance to blast. Sci. Rep. 4: 4550.
  21. 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
  22. Giatgong, P. and Frederiksen, R. A. 1968. Pathogenic variability and cytology of monoconidial subcultures of Pyricularia oryzae. Phytopathology 59: 1152-1157.
  23. Hamer, J. E., Farrall, L., Orbach, M. J., Valent, B. and Chumley, F. G. 1989. Host species-specific conservation of a family of repeated DNA sequences in the genome of a fungal plant pathogen. Proc. Natl. Acad. Sci. U.S.A. 86: 9981-9985. https://doi.org/10.1073/pnas.86.24.9981
  24. Hammond-Kosack, K. E. and Jones, J. D. 1997. Plant disease resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 575-607. https://doi.org/10.1146/annurev.arplant.48.1.575
  25. Hammond-Kosack, K. E. and Parker, J. E. 2003. Deciphering plantpathogen communication: fresh perspectives for molecular resistance breeding. Curr. Opin. Biotechnol. 14: 177-193. https://doi.org/10.1016/S0958-1669(03)00035-1
  26. Jia, Y., McAdams, S. A., Bryan, G. T., Hershey, H. P. and Valent, B. 2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19: 4004-4014. https://doi.org/10.1093/emboj/19.15.4004
  27. 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
  28. Kameswar Row, K. V. S. R., Aist, J. R. and Crill, J. P. 1985. Mitosis in the rice blast fungus and its possible implications for pathogenic variability. Can. J. Bot. 63: 1129-1134. https://doi.org/10.1139/b85-155
  29. 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
  30. 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
  31. Kiyosawa, S. 1982. Genetic and epidemiological modeling of breakdown of plant disease resistance. Annu. Rev. Phytopathol. 20: 93-117. https://doi.org/10.1146/annurev.py.20.090182.000521
  32. Kolmer, J. A. 1989. Virulence and race dynamics of Puccinia recondita f. sp. tritici in Canada during 1956-1987. Phytopathology 79: 349-356. https://doi.org/10.1094/Phyto-79-349
  33. Kumar, J., Nelson, R. J. and Zeigler, R. S. 1999. Population structure and dynamics of Magnaporthe grisea in the Indian Himalayas. Genetics 152: 971-984. https://doi.org/10.1093/genetics/152.3.971
  34. Le, M. T., Arie, T. and Teraoka, T. 2010. Population dynamics and pathogenic races of rice blast fungus, Magnaporthe oryzae in the Mekong Delta in Vietnam. J. Gen. Plant Pathol 76: 177-182. https://doi.org/10.1007/s10327-010-0231-8
  35. Leach, J. E., Vera Cruz, C. M., Bai, J. and Leung, H. 2001. Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annu. Rev. Phytopathol. 39: 187-224. https://doi.org/10.1146/annurev.phyto.39.1.187
  36. Liang, Y., Yan, B.-Y., Pen, Y.-L., Ji, Z.-J., Zeng, Y.-X., Wu, H.-L. et al. 2017. Molecular screening of blast resistance genes in rice germplasms resistant to Magnaporthe oryzae. Rice Sci. 24: 41-47. https://doi.org/10.1016/j.rsci.2016.07.004
  37. Ma, J., Lei, C., Xu, X., Hao, K., Wang, J., Cheng, Z. et al. 2015. Pi64, Encoding a novel CC-NBS-LRR protein, confers resistance to leaf and neck blast in rice. Mol. Plant-Microbe Interact. 28: 558-568. https://doi.org/10.1094/MPMI-11-14-0367-R
  38. Matsumoto, K., Yamaguchi, M. and Ichishima, E. 1994. Molecular cloning and nucleotide sequence of the complementary DNA for penicillolysin gene, plnC, and 18 kDa metalloendopeptidase gene from Penicillium citrinum. Biochim. Biophys. Acta 1218: 469-472. https://doi.org/10.1016/0167-4781(94)90209-7
  39. McDonald, B. A., McDermott, J. M., Goodwin, S. B. and Allard, R. W. 1989. The population biology of host-pathogen interaction. Annu. Rev. Phytopathol. 27: 77-94. https://doi.org/10.1146/annurev.py.27.090189.000453
  40. Mehdy, M. C. 1994. Active oxygen species in plant defense against pathogens. Plant Physiol. 105: 467-472. https://doi.org/10.1104/pp.105.2.467
  41. Mundt, C. C. 1990. Probability of mutation to multiple virulence and durability of resistance gene pyramids. Phytopathology 80: 221-223. https://doi.org/10.1094/Phyto-80-221
  42. Orbach, M. J., Farrall, L., Sweigard, J. A., Chumley, F. G. and Valent, B. 2000. A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell 12: 2019-2032. https://doi.org/10.1105/tpc.12.11.2019
  43. Ou, S. H. 1980. Pathogen variability and host resistance in rice blast disease. Annu. Rev. Phytopathol. 18: 167-187. https://doi.org/10.1146/annurev.py.18.090180.001123
  44. Ou, S. H. and Ayad, M. R. 1968. Pathogenic races of Pyricularia oryzae originating from single lesions and monoconidial cultures. Phytopathology 58: 179-182.
  45. Ou, S. H., Nuque, F. L., Ebron, T. T. and Awoderu, V. 1970. Pathogenic races of Pyricularia oryzae derived from monoconidial cultures. Plant Dis. Rep. 54: 1045-1049.
  46. 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
  47. Roumen, E., Levy, M. and Notteghem, J. L. 1997. Characterization of the European pathogen population of Magnaporthe grisea by DNA fingerprinting and pathotype analysis. Eur. J. Plant Pathol. 103: 363-371. https://doi.org/10.1023/A:1008697728788
  48. Shull, V. and Hamer, J. E. 1994. Genomic structure and variability in Magnaporthe grisea. In: Rice blast disease, eds. by R. S. Zeigler, S. A. Leong and P. S. Teng, pp. 65-86. CAB International, Wallingford, UK.
  49. Silue, D., Notteghem, J. L. and Tharreau, D. 1992a. Evidence of a gene-for-gene relationship in the Oryza sativa-Magnaporthe grisea pathosystem. Phytopathology 82: 577-580. https://doi.org/10.1094/Phyto-82-577
  50. Silue, D., Tharreau, D. and Notteghem, J. L. 1992b. Identification of Magnaporthe grisea avirulence genes to seven rice cultivars. Phytopathology 82: 1462-1467. https://doi.org/10.1094/Phyto-82-1462
  51. Suzuki, H. 1965. Origin of variation in Pyricularia oryzae. In: The rice blast disease, ed. by S. H. Ou, pp. 111-149. Johns Hopkins Press, Baltimore, Maryland, USA.
  52. Tatsumi, H., Murakami, S., Tsuji, R. F., Ishida, Y., Murakami, K., Masaki, A. et al. 1991. Cloning and expression in yeast of a cDNA clone encoding Aspergillus oryzae neutral protease II, a unique metalloprotease. Mol. Gen. Genet. 228: 97-103. https://doi.org/10.1007/BF00282453
  53. Valent, B. 1997. The rice blast fungus, Magnaporthe grisea. In: Plant Relationships Part B., eds. by G. C. Carroll and P. Tudzynski, pp. 37-54. Springer-Verlag, Berlin, Germany.
  54. Valent, B. and Chumley, F. G. 1994. Avirulence genes and mechanisms of genetic instability in the rice blast fungus. In: Rice blast disease, eds. by R. S. Zeigler, S. A. Leong and P. S. Teng, pp. 111-134. CAB International, Wallingford, UK.
  55. Wang, G. L. and Valent, B. 2017. Durable resistance to rice blast. Science 355: 906-907. https://doi.org/10.1126/science.aam9517
  56. Zeigler, R. S., Cuoc, L. X., Scott, R. P., Bernardo, M. A., Chen, D. H., Valent, B. et al. 1995. The relationship between lineage and virulence in Pyricularia grisea in the Philippines. Phytopathology 85: 443-451. https://doi.org/10.1094/Phyto-85-443
  57. Zhou, E., Jia, Y., Singh, P., Correll, J. C. 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