Multiple translocation of the avr-pita effector gene among chromosomes of the rice blast fungus magnaporthe oryzae and related species

PLoS Pathogens

Volumn 7, Issue 7, 2011, Pages

  Chuma, Izumi ^a   Isobe, Chihiro ^a   Hotta, Yuma ^a   Ibaragi, Kana ^a   Futamata, Natsuru ^a   Kusaba, Motoaki ^b   Yoshida, Kentaro ^c   Terauchi, Ryohei ^c   Fujita, Yoshikatsu ^d   Nakayashiki, Hitoshi ^a   Valent, Barbara ^e   Tosa, Yukio ^a  

^a KOBE UNIVERSITY   (Japan)

^b SAGA UNIVERSITY   (Japan)

^c IWATE BIOTECHNOLOGY RESEARCH CENTER   (Japan)

^d NATIONAL AGRICULTURAL RESEARCH CENTER   (Japan)

^e KANSAS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AVR PITA1 PROTEIN; AVR PITA2 PROTEIN; FUNGAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ASEXUAL REPRODUCTION; CHROMOSOME; CHROMOSOME 1; CHROMOSOME 2; CHROMOSOME 4; CHROMOSOME 6; CHROMOSOME 7; CHROMOSOME REARRANGEMENT; CHROMOSOME TRANSLOCATION; FUNGAL GENOME; FUNGAL VIRULENCE; FUNGUS; GENETIC POLYMORPHISM; MAGNAPORTHE ORYZAE; NONHUMAN; NUCLEOTIDE SEQUENCE; RICE; TELOMERE; BIOSYNTHESIS; FUNGAL GENE; GENE EXPRESSION REGULATION; GENETICS; MAGNAPORTHE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; PLANT DISEASE;

FUNGI; MAGNAPORTHE GRISEA; MAGNAPORTHE ORYZAE; TRITICUM AESTIVUM;

BASE SEQUENCE; CHROMOSOMES, FUNGAL; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; GENOME, FUNGAL; MAGNAPORTHE; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; PLANT DISEASES;

EID: 79960957443     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002147     Document Type: Article

References (95)

1. Heath MC, (1981) A generalized concept of host-parasite specificity. Phytopathology 71: 1121-1123.
2. Kiyosawa S, (1982) Genetics and epidemiological modeling of breakdown of plant disease resistance. Ann Rev Phytopathol 20: 93-117.
3. Leach JE, Cruz CMV, Bai J, Leung H, (2001) Pathogen fitness penalty as a predictor of durability of disease resistance genes. Ann Rev Phytopathol 39: 187-224.
4. McDonald BA, Linde C, (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Ann Rev Phytopathol 40: 349-379.
5. Flor HH, (1956) The complementary genic systems in flax and flax rust. Adv Genet 8: 29-54.
6. Fudal I, Ross S, Brun H, Besnard A-L, Ermel M, et al. (2009) Repeat-induced point mutation (RIP) as an alternative mechanism of evolution toward virulence in Leptosphaeria maculans. Mol Plant-Microbe Interact 22: 932-941.
7. Van de Wouw AP, Cozijnsen AJ, Hane JK, Brunner PC, McDonald BA, et al. (2010) Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathog 6: e1001180.
8. De Wit PJGM, Mehrabi R, van den Burg HA, Stergiopoulos I, (2009) Fungal effector proteins: past, present and future. Mol Plant Pathol 10: 735-747.
9. Gout L, Kuhn ML, Vincenot L, Bernard-Samain S, Cattolico L, et al. (2007) Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Envion Microbiol 9: 2978-2992.
10. Schürch S, Linde CC, Knogge W, Jackson LF, McDonald BA, (2004) Molecular population genetic analysis differentiates two virulence mechanisms of the fungal avirulence gene NIP1. Mol Plant-Microbe Interact 17: 1114-1125.
11. Kiyosawa S, Ando I, Ishiguro K, Nemoto F, Hashimoto A, (1991) Three examples of yearly change of frequencies of unnecessary virulence genes under field conditions where resistance genes for rice blast are not present. Bull Fukushima Pref Agri Exp Stn 30: 23-36.
12. Hirata K, Kusaba M, Chuma I, Osue J, Nakayashiki H, et al. (2007) Speciation in Pyricularia inferred from multilocus phylogenetic analysis. Mycol Res 111: 799-808.
13. Kato H, Yamamoto M, Yamaguchi-Ozaki T, Kadouchi H, Iwamoto Y, et al. (2000) Pathogenicity, mating ability and DNA restriction fragment length polymorphisms of Pyricularia populations isolated from Gramineae, Bambusideae and Zingiberaceae plants. J Gen Plant Pathol 66: 30-47.
14. Couch BC, Kohn LM, (2002) A multilocus gene genealogy concordant with host preference indicates segregation of a new species, Magnaporthe oryzae, from M. grisea. Mycologia 94: 683-693.
15. Tosa Y, Hirata K, Tamba H, Nakagawa S, Chuma I, et al. (2004) Genetic constitution and pathogenicity of Lolium isolates of Magnaporthe oryzae in comparison with host species-specific pathotypes of the blast fungus. Phytopathology 94: 454-462.
16. Kato H, (1983) Responses of Italian millet, oat, timothy, Italian ryegrass and perennial ryegrass to Pyricularia species isolated from cereals and grasses. Proc Kanto-Tosan Plant Prot Soc 30: 22-23 (In Japanese).
17. Zeigler RS, Scott RP, Leung H, Bordeos AA, Kumar J, et al. (1997) Evidence of parasexual exchange of DNA in the rice blast fungus challenges its exclusive clonality. Phytopathology 87: 284-294.
18. Kato H, Yamaguchi T, Nishihara N, (1976) The perfect state of Pyricularia oryzae Cav. in culture. Ann Phytopathol Soc Jpn 42: 507-510.
19. Yaegashi H, Nishihara N, (1976) Production of the perfect stage in Pyricularia from cereals and grasses. Ann Phytopathol Soc Jpn 42: 511-515.
20. Ueyama A, Tsuda M, (1975) Formation of the perfect state in culture of Pyricularia sp. from some graminaceous plants (preliminary report). Trans Mycol Soc Jpn 16: 420-422.
21. Takabayashi N, Tosa Y, Oh HS, Mayama S, (2002) A gene-for-gene relationship underlying the species-specific parasitism of Avena/Triticum isolates of Magnaporthe grisea on wheat cultivars. Phytopathology 92: 1182-1188.
22. Tosa Y, Tamba H, Tanaka K, Mayama S, (2006) Genetic analysis of host species specificity of Magnaporthe oryzae isolates from rice and wheat. Phytopathology 96: 480-484.
23. Valent B, Khang CH, (2010) Recent advances in rice blast effector research. Curr Opin Plant Biol 13: 434-441.
24. Silue D, Notteghem JL, Tharreau D, (1992) Evidence of a gene-for-gene relationship in the Oryza sativa - Magnaporthe grisea pathosystem. Phytopathology 82: 577-580.
25. Kang S, Sweigard JA, Valent B, (1995) The PWL host specificity gene family in the blast fungus Magnaporthe grisea. Mol Plant-Microbe Interact 8: 939-948.
26. Sweigard JA, Carroll AM, Kang S, Farrall L, Chumley FG, et al. (1995) Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. Plant Cell 7: 1221-1233.
27. Farman ML, Leong SA, (1998) Chromosome walking to the AVR1-CO39 avirulence gene of Magnaporthe grisea: Discrepancy between the physical and genetic maps. Genetics 150: 1049-1058.
28. Orbach MJ, Farrall L, Sweigard JA, Chumley FG, Valent B, (2000) A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell 12: 2019-2032.
29. Böhnert HU, Fudal I, Dioh W, Tharreau D, Notteghem J-L, et al. (2004) A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistance rice. Plant Cell 16: 2499-2513.
30. Li W, Wang B, Wu J, Lu G, Hu Y, et al. (2009) The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Mol Plant-Microbe Interact 22: 411-420.
31. Miki S, Matsui K, Kito H, Otsuka K, Ashizawa T, et al. (2009) Molecular cloning and characterization of the AVR-Pia locus from a Japanese field isolate of Magnaporthe oryzae. Mol Plant Pathol 10: 361-374.
32. Yoshida K, Saitoh H, Fujisawa S, Kanzaki H, Matsumura H, et al. (2009) Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell 21: 1573-1591.
33. Dai Y, Jia Y, Correll J, Wang X, Wang Y, (2010) Diversification and evolution of the avirulence gene AVR-Pita1 in field isolates of Magnaporthe oryzae. Fun Genet Biol 37: 973-980.
34. Kang S, Lebrun MH, Farrall L, 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.
35. Takahashi M, Ashizawa T, Hirayae K, Moriwaki J, Sone T, et al. (2010) One of two major paralogs of AVR-Pita1 is functional in Japanese rice blast isolates. Phytopathology 100: 612-618.
36. Zhou E, Jia Y, Singh P, Correll JC, Lee FN, (2007) Instability of the Magnaporthe oryzae avirulence gene AVR-Pita alters virulence. Fungal Genet Biol 44: 1024-1034.
37. Bryan GT, Wu KS, Farrall L, Jia Y, Hershey HP, et al. (2000) A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell 12: 2033-2045.
38. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B, (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19: 4004-4014.
39. Khang CH, Park S-Y, Lee Y-H, Valent B, 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.
40. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, et al. (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309: 416-422.
41. Dreesen O, Li B, Cross GAM, (2007) Telomere structure and function in trypanosomes: a proposal. Nat Rev Microbiol 5: 70-75.
42. Taylor JE, Rudenko G, (2006) Switching trypanosome coats: what's in the wardrobe? Trends in Genet 22: 614-620.
43. Gardner MJ, Hall N, Fung E, White O, Berriman M, et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
44. Freitas-Junior LH, Bottius E, Pirrit LA, Deitsch KW, Scheidig C, et al. (2000) Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407: 1018-1022.
45. Luo CX, Hanamura H, Sezaki H, Kusaba M, Yaegashi H, (2002) Relationship between avirulence genes of the same family in rice blast fungus Magnaporthe grisea. J Gen Plant Pathol 68: 300-306.
46. Luo CX, Yin LF, Koyanagi S, Farman ML, Kusaba M, et al. (2005) Genetic mapping and chromosomal assignment of Magnaporthe oryzae avirulence genes AvrPik, AvrPiz, and AvrPiz-t controlling cultivar specificity on rice. Phytopathology 95: 640-647.
47. Nitta N, Farman ML, Leong SA, (1997) Genome organization of Magnaporthe grisea: integration of genetic maps, clustering of transposable elements and identification of genome duplications and rearrangements. Theor Appl Genet 95: 20-32.
48. Chuma I, Tosa Y, Taga M, Nakayashiki H, Mayama S, (2003) Meiotic behavior of a supernumerary chromosome in Magnaporthe oryzae. Curr Genet 43: 191-198.
49. Orbach MJ, Chumley FG, Valent B, (1996) Electrophoretic karyotypes of Magnaporthe grisea pathogens of diverse grasses. Mol Plant-Microbe Interact 9: 261-271.
50. Talbot NJ, Salch YP, Ma M, Hamer JE, (1993) Karyotypic variation within clonal lineages of the rice blast fungus, Magnaporthe grisea. Appl Environ Microbiol 59: 585-593.
51. Chuma I, Zhan S-W, Asano S, Nga NTT, Vy TTP, et al. (2010) PWT1, an avirulence gene of Magnaporthe oryzae tightly linked to the rDNA locus, is recognized by two staple crops, common wheat and barley. Phytopathology 100: 436-443.
52. Zheng Y, Zhang G, Lin F, Wang Z, Jin G, et al. (2008) Development of microsatellite markers and construction of genetic map in rice blast pathogen Magnaporthe grisea. Fungal Genet Biol 45: 1340-1347.
53. Nakayashiki H, Matsuo H, Chuma I, Ikeda K, Betsuyaku S, et al. (2001) Pyret, a Ty3/gypsy retrotransposon in Magnaporthe grisea contains an extra domain between the nucleocapsid and protease domains. Nucleic Acids Res 29: 4106-4113.
54. Kang S, (2001) Organization and distribution pattern of MGLR-3, a novel retrotransposon in the rice blast fungus Magnaporthe grisea. Fungal Genet Biol 32: 11-19.
55. Hamer JE, Farrall L, Orbach MJ, Valent B, Chumley FG, (1989) Host species-specific conservation of a family of repeated DNA sequences in the genome of a fungal plant pathogen. Proc Natl Acad Sci USA 86: 9981-9985.
56. Kachroo P, Ahuja M, Leong SA, Chattoo BB, (1997) Organization and molecular analysis of repeated DNA sequences in the rice blast fungus Magnaporthe grisea. Curr Genet 31: 361-369.
57. Kachroo P, Leong SA, Chattoo BB, (1994) Pot2, an inverted repeat transposon from the rice blast fungus Magnaporthe grisea. Mol Gen Genet 245: 339-348.
58. Farman ML, Taura S, Leong SA, (1996) The Maganaporthe grisea DNA fingerprinting probe MGR586 contains the 3' end of an inverted repeat transposon. Mol Gen Genet 251: 675-681.
59. Kito H, Takahashi Y, Sato J, Fukiya S, Sone T, et al. (2003) Occan, a novel transposon in the Fot1 family, is ubiquitously found in several Magnaporthe grisea isolates. Curr Genet 42: 322-331.
60. Farman ML, Tosa Y, Nitta N, Leong SA, (1996) MAGGY, a retrotransposon in the genome of the rice blast fungus Magnaporthe grisea. Mol Gen Genet 251: 665-674.
61. Aboukhaddour R, Cloutier S, Ballance GM, Lamari L, (2009) Genome characterization of Pyrenophora tritici-repentis isolates reveals high plasticity and independent chromosomal location of ToxA and ToxB. Mol Plant Pathol 10: 201-212.
62. Mieczkowski PA, Lemoine FJ, Petes TD, (2006) Recombination between retrotransposons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae. DNA repair 5: 1010-1020.
63. Van der Plank JE, (1984) Disease Resistance in Plants. Academic Press, Inc.
64. Murata S, Takasaki N, Saitoh M, Okada N, (1993) Determination of the phylogenetic relationships among Pacific salmonids by using short interspersed elements (SINEs) as temporal landmarks of evolution. Proc Natl Acad Sci USA 90: 6995-6999.
65. Covert SF, (1998) Supernumerary chromosomes in filamentous fungi. Curr Genet 33: 311-319.
66. Miao VP, Covert SF, VanEtten HD, (1991) A fungal gene for antibiotic resistance on a dispensable ("B") chromosome. Science 254: 1773-1776.
67. Han Y, Liu X, Benny U, Kistler C, VanEtten HD, (2001) Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. Plant J 25: 305-314.
68. Akagi Y, Akamatsu H, Otani H, Kodama M, (2009) Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot Cell 8: 1732-1738.
69. Hatta R, Ito K, Hosaki Y, Tanaka T, Tanaka A, et al. (2002) A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161: 59-70.
70. Johnson LJ, Johnson RD, Akamatsu H, Salamiah A, Otani H, et al. (2001) Spontaneous loss of a conditionally dispensable chromosome from the Alternaria alternata apple pathotype leads to loss of toxin production and pathogenicity. Curr Genet 40: 65-72.
71. Masunaka A, Ohtani K, Peever TL, Timmer LW, Tsuge T, et al. (2005) An isolate of Alternaria alternata that is pathogenic to both tangerines and rough lemon and produces two host-selective toxins, ACT- and ACR-toxins. Phytopathology 95: 241-247.
72. Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC, et al. (2009) The genome of Nectria haematococca: Contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5: e1000618.
73. He C, Rusu AG, Poplawski AM, Irwin JAG, Manners JM, (1998) Transfer of a supernumerary chromosome between vegetatively incompatible biotypes of the fungus Colletotrichum gloeosporioides. Genetics 150: 1459-1466.
74. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, et al. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367-373.
75. Noguchi MT, Yasuda N, 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.
76. Yasuda N, Tsujimoto-Noguchi M, Fujita Y, (2006) Partial mapping of avirulence genes AVR-Pii and AVR-Pia in the rice blast fungus Magnaporthe oryzae. Can J Plant Pathol 28: 494-498.
77. Chen QH, Wang YC, Li AN, Zhang ZG, Zheng XB, (2007) Molecular mapping of two cultivar-specific avirulence genes in the rice blast fungus Magnaporthe grisea. Mol Genet Genomics 277: 139-148.
78. Feng S, Ma J, Lin F, Wang L, Pan Q, (2007) Construction of an electronic physical map of Magnaporthe oryzae using genomic position-ready SSR markers. Chin Sci Bull 52: 3346-3354.
79. Luo CX, Yin LF, Ohtaka K, Kusaba M, (2007) The 1.6 Mb chromosome carrying the avirulence gene AvrPik in Magnaporthe oryzae isolate 84R-62B is a chimera containing chromosome 1 sequences. Mycol Res 111: 232-239.
80. Jones JDG, Dangl JL, (2006) The plant immune system. Nature 444: 323-329.
81. Carlson M, Celenza JL, Eng FJ, (1985) Evolution of the dispersed SUC gene family of Saccharomyces by rearrangements of chromosome telomeres. Mol Cell Biol 5: 2894-2902.
82. Charron MJ, Read E, Haut SR, Michels CA, (1989) Molecular evolution of the telomere-associated MAL loci of Saccharomyces. Genetics 122: 307-316.
83. Brown CA, Murray AW, Verstrepen KJ, (2010) Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Curr Biol 20: 895-903.
84. Dioh W, Tharreau D, Notteghem JL, Orbach MJ, Lebrun M-H, (2000) Mapping of avirulence genes in the rice blast fungus, Magnaporthe grisea, with RFLP and RAPD markers. Mol Plant-Microbe Interact 13: 217-227.
85. Farman ML, (2007) Telomeres in the rice blast fungus Magnaporthe oryzae: the world of the end as we know it. FEMS Microbiol Lett 273: 125-132.
86. Valent B, Chumley FG, (1994) Avirulence genes and mechanisms of genetic instability in the rice blast fungus. In: Zeigler RS, Leong SA, Teng PS, editors. The Rice Blast Disease Cambridge International Rice Research Institute, Los Banos and Commonwealth Agricultural Bureaux pp. 111-134 Chapter 7.
87. Rehmeyer C, Li W, Kusaba M, Kim Y-S, Brown D, et al. (2006) Organization of chromosome ends in the rice blast fungus, Magnaporthe oryzae. Nucl Acid Res 34: 4685-4701.
88. Verstrepen KK, Fink GR, (2009) Genetic and epigenetic mechanisms underlying cell-surface variability in protozoa and fungi. Annu Rev Genet 43: 1-24.
89. Murakami J, Tosa Y, Kataoka T, Tomita R, Kawasaki J, et al. (2000) Analysis of host species specificity of Magnaporthe grisea toward wheat using a genetic cross between isolates from wheat and foxtail millet. Phytopathology 90: 1060-1067.
90. Nakayashiki H, Kiyotomi K, Tosa Y, Mayama S, (1999) Transposition of the retrotransposon MAGGY in heterologous species of filamentous fungi. Genetics 153: 693-703.
91. Römling U, Tümmler B, (2000) Achieving 100% type ability of Pseudomonas aeruginosa by pulsed-field gel electrophoresis. J Clin Microbiol 38: 464-465.
92. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol Biol Evol 24: 1596-1599.
93. Kimura N, Tsuge T, (1993) Gene cluster involved in melanin biosynthesis of the filamentous fungus Alternaria alternata. J Bacteriol 175: 4427-4435.
94. Tosa Y, Osue J, Eto Y, Oh H, Nakayashiki H, et al. (2005) Evolution of an avirulence gene, AVR1-CO39, concomitant with the evolution and differentiation of Magnaporthe oryzae. Mol Plant-Microbe Interact 18: 1148-1160.
95. Ronquist F, Hülsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.