Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions

Plant Journal

Volumn 72, Issue 6, 2012, Pages 894-907

  Kanzaki, Hiroyuki ^a   Yoshida, Kentaro ^a   Saitoh, Hiromasa ^a   Fujisaki, Koki ^a   Hirabuchi, Akiko ^a   Alaux, Ludovic ^b,c   Fournier, Elisabeth ^b   Tharreau, Didier ^c   Terauchi, Ryohei ^a  

^a IWATE BIOTECHNOLOGY RESEARCH CENTER   (Japan)

^b Campus International de Baillarguet   (France)

^c CIRAD   (France)

Author keywords

Arms race; Avirulence gene; Coevolution; Magnaporthe oryzae; Oryza sativa; Population genetics; Resistance gene

Indexed keywords

ARMS RACE; AVIRULENCE; CO-EVOLUTION; MAGNAPORTHE ORYZAE; ORYZA SATIVA; POPULATION GENETICS; RESISTANCE GENES;

AMINO ACIDS; BINS;

GENES;

MAGNAPORTHE ORYZAE; ORYZA SATIVA;

FUNGAL PROTEIN; VEGETABLE PROTEIN;

ALLELE; AMINO ACID SEQUENCE; BIOLOGICAL MODEL; DISEASE RESISTANCE; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; MAGNAPORTHE; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; MUTATION; PATHOGENICITY; PLANT DISEASE; PROTEIN TERTIARY STRUCTURE; RICE; TWO HYBRID SYSTEM; VIRULENCE;

ALLELES; AMINO ACID SEQUENCE; DISEASE RESISTANCE; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; MAGNAPORTHE; MODELS, BIOLOGICAL; MUTATION; ORYZA SATIVA; PLANT DISEASES; PLANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, DNA; TWO-HYBRID SYSTEM TECHNIQUES; VIRULENCE;

EID: 84871961578     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.05110.x     Document Type: Article

References (48)

1. Allen, R.L., Bitter-Eddy, P.D., Grenville-Briggs, L.J., Meitz, J.C., Rehmany, A.P., Rose, L.E. and Beynon, J.L. (2004) Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science, 306,1957-1960.
2. Ashikawa, I., Hayashi, N., Yamane, H., Kanamori, H., Wu, J., Matsumoto, T., Ono, K. and Yano, M. (2008) Two adjacent nucleotide-binding site-leucinerich repeat class genes are required to confer Pikm-specific rice blast resistance. Genetics, 180, 2267-2276.
3. Ashikawa, I., Wu, J., Matsumoto, T. and Ishikawa, R. (2010) Haplotype diversity and molecular evolution of the rice Pikm locus for blast resistance. J. Gen. Plant Pathol. 76, 37-42.
4. Ballini, E., Morel, J.-B., Droc, G., Price, A., Courtois, B., Notteghem, J.-L. and Tharreau, D. (2008) A genome-wide meta-analysis of rice blast resistance genes and QTLs provides new insights into partial and complete resistance. Mol. Plant Microbe Interact. 21, 859-868.
5. Barrett, L.G., Thrall, P.H., Dodds, P.N., van der Merwe, M., Linde, C.C., Lawrence, G.J. and Burdon, J.J. (2009) Diversity and evolution of effector loci in natural populations of the plant pathogen Melampsora lini. Mol. Biol. Evol. 26, 2499-2513.
6. Böhnert, H.U., Fudal, I., Dioh, W., Tharreau, D., Nottéghem, J.-L. and Lebrun, M.-H. (2004) A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistant rice. Plant Cell, 16, 2499-2513.
7. Chen, Y., Liu, Z. and Halterman, D.A. (2012) Molecular determinants of resistance activation and suppression by Phytophthora infestans effector IPI-O. PLoS Pathog. 8, e1002595.
8. Christensen, A.H. and Quail, P.H. (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Res. 5, 213-218.
9. Chuma, I., Isobe, C., Hotta, Y. et al. (2011) Multiple translocation of the AVRPita effector gene among chromosomes of the rice blast fungus Magnaporthe oryzae and related species. PLoS Pathog. 7, e1002147.
10. Constanzo, S. and Jia, Y. (2010) Sequence variation at the rice blast gene Pikm locus: implications for the development of allele specific markers. Plant Sci. 178, 523-530.
11. Dai, Y., Jia, Y., Correll, J., Wang, X. and Wang, Y. (2010) Diversification and evolution of the avirulence gene AVR-Pita1 in field isolates of Magnaporthe oryzae. Fungal Genet. Biol. 47, 973-980.
12. Dangl, J.L. and Jones, J.D. (2001) Plant pathogens and integrated defence responses to infection. Nature, 411, 826-833.
13. Dodds, P.N., Lawrence, G.J., Catanzariti, A.M., Ayliffe, M.A. and Ellis, J.G. (2004) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell, 15, 755-768.
14. Dodds, P.N., Lawrence, G.J., Catanzariti, A.-M., Teh, T., Wang, A.-I., Ayliffe, M.A., Kobe, B. and Ellis, J.G. (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. USA, 103, 8888-8893.
15. Ebert, D. and Hamilton, W.D. (1996) Sex against virulence: the coevolution of parasitic diseases. Trends Ecol. Evol. 11, 79-82.
16. Ellis, J.G., Lawrence, G.J., Luck, J.E. and Dodds, P.N. (1999) Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell, 11, 495-506.
17. Flor, H.H. (1956) The complementary genic systems in flax and flax rust. Adv. Genet. 8, 29-54.
18. Haldane, J.B.S. (1949) Disease and evolution. Ric. Sci. Suppl. 19, 68-76.
19. 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.
20. Jukes, T.H. and Cantor, C.R. (1969) Evolution of protein molecules. In Mammalian Protein Metabolism (Munro, H.N., ed). New York, NY: Academic Press, pp. 21-132.
21. Kanzaki, H., Nirasawa, S., Saitoh, H., Ito, M., Nishihara, M., Terauchi, R. and Nakamura, I. (2002) Overexpression of the wasabi defensin gene confers enhanced resistance to blast fungus (Magnaporthe grisea) in transgenic rice. Theor. Appl. Genet. 105, 809-814.
22. Kojima, Y., Ebana, K., Fukuoka, S., Nagamine, T. and Kawase, M. (2005) Development of an RFLP-based rice diversity research set of germplasm. Breed. Sci. 55, 431-440.
23. Krasileva, K.V., Dahlbeck, D. and Staskawicz, B.J. (2010) Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell, 22, 2444-2458.
24. Li, W., Wang, B., Wu, J. 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.
25. Librado, P. and Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
26. Liu, J., Wang, X., Mitchell, T., Hu, Y., Liu, X., Dai, L. and Wang, G.-L. (2010) Recent progress and understanding of the molecular mechanisms of the rice-Magnaporthe oryzae interaction. Mol. Plant Pathol. 211, 419-427.
27. Morran, L.T., Schmidt, O.G., Galarden, A.I., Parrish, R.C. II and Liverly, C.M. (2011) Running with the Red Queen: host-parasite coevolution selects for biparental sex. Science, 333, 216-218.
28. Nei, M. (1987) Molecular Evolutionary Genetics. New York, NY: Columbia University Press.
29. Nei, M. and Kumar, S. (2000) Molecular Evolution and Phylogenetics. New York, NY: Oxford University Press.
30. 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.
31. Rairdan, G.J. and Moffett, P. (2006) Distinct domains in the ARC region of the potato resistance protein Rx mediate LRR binding and inhibition of activation. Plant Cell, 18, 2082-2093.
32. Ravensdale, M., Nemri, A., Thrall, P.H., Ellis, J.G. and Dodds, P.N. (2011) Coevolutionary interactions between host resistance and pathogen effector genes in flax rust disease. Mol. Plant Pathol. 12, 93-102.
33. Rose, L.E., Bittner-Eddy, P.D., Langley, C.H., Holub, E.B., Michelmore, R.W. and Beynon, J.L. (2004) The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics, 166, 1517-1527.
34. Saleh, D., Xu, P., Shen, Y., Li, C.Y., Adreit, H., Milazzo, J., Ravigné, V. and Bazin, E. (2012) Sex at the origin: an Asian population of the rice blast fungus Magnaporthe oryzae reproduces sexually. Mol. Ecol. 21,1330-1344.
35. Shen, Q.-H., Zhou, F., Bieri, S., Haizel, T., Shirasu, K. and Shulze-Lefert, P. (2003) Recognition specificity and RAR1/SGT1 dependence in barley Mla disease resistance genes to the powdery mildew fungus. Plant Cell, 15, 732-744.
36. Stahl, E.A., Dwyer, G., Mauricio, R., Kreitman, M. and Bergelson, J. (1999) Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature, 400, 667-671.
37. Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595.
38. Takahashi, M., Ashizawa, T., Hirayae, K., Moriwaki, J., Sone, T., Sonoda, R., Noguchi, M.T., Nagashima, S., Ishikawa, K. and Arai, M. (2010) One of two major paralogs of AVR-Pita1 is functional in Japanese rice blast isolates. Phytopathology, 100, 612-618.
39. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739.
40. Terauchi, R. and Yoshida, K. (2010) Towards population genomics of effector-effector target interactions. New Phytol. 187, 929-939.
41. Terauchi, R., Yoshida, K., Saitoh, H., Kanzaki, H., Okuyama, Y., Fujisaki, K., Miya, A., Abe, A., Tamiru, M. and Tosa, Y. (2011) Studying genome-wide DNA polymorphisms to understand Magnaporthe-rice interactions. Aust. Plant Pathol. 40, 328-334.
42. Tharreau, D., Fudal, I., Andriantsimialona, D., Santoso, Utami, D., Fournier, E., Lebrun, M.-H. and Nottéghem, J.-L. (2009) World population structure and migration of the rice blast fungus, Magnaporthe oryzae. In Advances in Genetics, Genomics and Control of Rice Blast Disease (Wang, G.-L. and Valent, B., eds). New York: Springer Verlag, pp. 209-215.
43. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
44. Win, J., Kamoun, S. and Jones, A.M.E. (2011) Purification of effector-target complexes via transient expression in Nicotiana benthamiana. Methods Mol. Biol. 712, 181-193.
45. Woolhouse, M.E., Webster, J.P., Domingo, E., Charlesworth, B. and Levin, B.R. (2002) Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 32, 569-577.
46. Yoshida, K., Saitoh, H., Fujisawa, S. et al. (2009) Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell, 21, 1573-1591.
47. Zhai, C., Lin, F., Dong, Z., He, X., Yuan, B., Zeng, X., Wang, L. and Pan, Q. (2011) The isolation and characterization of Pik, a rice blast resistance gene which emerged after rice domestication. New Phytol. 189, 321-334.
48. 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.