A multifaceted genomics approach allows the isolation of the rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes

Plant Journal

Volumn 66, Issue 3, 2011, Pages 467-479

  Okuyama, Yudai ^a,b   Kanzaki, Hiroyuki ^a   Abe, Akira ^c   Yoshida, Kentaro ^a   Tamiru, Muluneh ^a   Saitoh, Hiromasa ^a   Fujibe, Takahiro ^a   Matsumura, Hideo ^a   Shenton, Matt ^a   Galam, Dominique Clark ^a   Undan, Jerwin ^a   Ito, Akiko ^a   Sone, Teruo ^d   Terauchi, Ryohei ^a  

^a IWATE BIOTECHNOLOGY RESEARCH CENTER   (Japan)

^b DEPARTMENT OF BOTANY   (Japan)

^c IWATE AGRICULTURAL RESEARCH CENTER   (Japan)

^d HOKKAIDO UNIVERSITY   (Japan)

Author keywords

association genetics; hypersensitive response; mutant screening; phylogenetics; protoplast assay

Indexed keywords

ASSOCIATION GENETICS; HYPERSENSITIVE RESPONSE; MUTANT SCREENING; PHYLOGENETICS; PROTOPLAST ASSAY;

AMINO ACIDS; CHROMOSOMES; CLONING; DNA SEQUENCES; FUNGUS RESISTANCE; GENE ENCODING; METHANE; NUCLEIC ACIDS;

BLAST RESISTANCE;

MESYLIC ACID ETHYL ESTER;

ALLELE; AMINO ACID SEQUENCE; ARTICLE; CHROMOSOME MAP; DRUG EFFECT; GENE ORDER; GENETIC COMPLEMENTATION; GENETIC POLYMORPHISM; GENETIC TRANSFECTION; GENETICS; GENOMICS; IMMUNOLOGY; INNATE IMMUNITY; MAGNAPORTHE; METABOLISM; METHODOLOGY; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; PATHOGENICITY; PHENOTYPE; PHYLOGENY; PLANT CHROMOSOME; PLANT DISEASE; PLANT GENE; POINT MUTATION; PROTOPLAST; RICE; TRANSGENE; TRANSGENIC PLANT;

ALLELES; AMINO ACID SEQUENCE; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; CLONING, MOLECULAR; ETHYL METHANESULFONATE; GENE ORDER; GENES, PLANT; GENETIC COMPLEMENTATION TEST; GENOMICS; IMMUNITY, INNATE; MAGNAPORTHE; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; PHENOTYPE; PHYLOGENY; PLANT DISEASES; PLANTS, GENETICALLY MODIFIED; POINT MUTATION; POLYMORPHISM, GENETIC; PROTOPLASTS; TRANSFECTION; TRANSGENES;

FUNGI; MAGNAPORTHE ORYZAE; ORYZA SATIVA;

EID: 79955402863     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04502.x     Document Type: Article

References (54)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and, Lipman, D.J., (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
2. Ashikawa, I., Hayashi, N., Yamane, H., Kanamori, H., Wu, J., Matsumoto, T., Ono, K., and, Yano, M., (2008) Two adjacent nucleotide-binding site-leucine-rich repeat class genes are required to confer Pikm-specific rice blast resistance. Genetics, 180, 2267-2276.
3. Bent, A.F., and, Mackey, D., (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45, 399-436. (Pubitemid 351321400)
4. Böhnert, H.U., Fudal, I., Dioh, W., Tharreau, D., Notteghem, 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. (Pubitemid 39247087)
5. Catanzariti, A.-M., Doddsa, P.N., Lawrencea, G.J., Ayliffea, M.A., and, Ellis, J.G., (2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell, 18, 243-256. (Pubitemid 43951327)
6. Chen, S., Tao, L., Zeng, L., Vega-Sanchez, M.E., Umemura, K., and, Wang, G.-L., (2006) A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice. Mol. Plant. Pathol. 7, 417-427. (Pubitemid 44337800)
7. 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. (Pubitemid 126603490)
8. Clark, R.M., Schweikert, G., Ossowski, S., et al. (2007) Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science, 317, 338-342. (Pubitemid 47106367)
9. Dangl, J.L., and, Jones, J.D.G., (2001) Plant pathogens and integrated defence responses to infection. Nature, 411, 826-833. (Pubitemid 32588110)
10. Dean, R.A., Talbot, N.J., Ebbole, D.J., et al. (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature, 434, 980-986. (Pubitemid 40586040)
11. Dodds, P.N., Fafiqi, M., Gan, P.H.P., Hardham, A.R., Jones, D.A., and, Ellis, J.G., (2009) Effectors of biotrophic fungi and oomycetes: pathogenicity factors and triggers of host resistance. New Phytol. 183, 993-1000.
12. Ellis, J.G., Dodds, P.N., and, Lawrence, G.J., (2007) The role of secreted proteins in diseases of plants caused by rust, powdery mildew and smut fungi. Curr. Opin. Microbiol. 10, 326-331. (Pubitemid 47404947)
13. Fouts, D.E., Abramovitch, R.B., Alfano, J.R., et al. (2002) Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc. Natl Acad. Sci. USA, 99, 2275-2280. (Pubitemid 34169051)
14. Fu, Y.-X., and, Li, W.-H., (1993) Statistical tests of neutrality of mutations. Genetics, 133, 693-709. (Pubitemid 23066572)
15. Hirschhorn, J.N., and, Daly, M.J., (2005) Genome-wide association studies for common diseases and complex traits. Nat. Rev. Genet. 6, 95-108. (Pubitemid 40179532)
16. Hogenhout, S.A., van der Hoorn, R.A.L., Terauchi, R., and, Kamoun, S., (2009) Emerging concepts in effector biology of plant-associated organisms. Mol.Plant-Microbe Interact. 22, 115-122.
17. van der Hoorn, A.A.L., De Wit, P.J.G.M., and, Joosten, M.H.A.J., (2002) Balancing selection favors guarding resistance proteins. Trends Plant Sci. 7, 67-71. (Pubitemid 36726075)
18. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature, 436, 793-800.
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. (Pubitemid 30608539)
20. Jones, J.D.G., and, Dangl, J.L., (2006) The plant immune system. Nature, 444, 323-329. (Pubitemid 44764102)
21. Kamoun, S., (2007) Groovy times: filamentous pathogen effectors revealed. Curr. Opin. Plant Biol. 10, 358-365. (Pubitemid 47126945)
22. 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. (Pubitemid 36080307)
23. Kataoka, T., Kato, H., Takita, T., Yokogami, N., and, Yamaguchi, M., (2004) Selection of criterional varieties for evaluation of blast partial resistance of rice in the Tohoku Region of Japan. In Rice blast: Interaction with Rice and Control (, Kawasaki, S., ed.). Proceedings of the 3rd International Rice Blast Conference, Tsukuba Science City, Ibaraki, Japan, pp. 123-129.
24. Kinoshita, T., (1998) Report from coordinator Linkage mapping using mutant genes in rice. In Rice Genetics Newsletter, Vol. 15 (, Sano, Y., and, Khush, G.S., eds). Japan: A Publication of the Rice Genetics Cooperative, pp. 13-74.
25. Kiyosawa, S., Mackill, D.J., Bonman, J.M., Tanaka, Y., and, Ling, Z.Z., (1986) An attempt of classification of world's rice varieties based on reaction pattern to blast fungus strains. Bull. Natl. Inst. Agrobiol. Resour. 2, 13-39.
26. Larkin, M.A., Blackshields, G., Brown, N.P., et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948. (Pubitemid 350162903)
27. Lee, S.-K., Song, M.-Y., Seo, Y.-S., et al. (2009) Rice Pi5-mediated resistance to Magnaporthe oryzae requires the presence of two coiled-coil-nucleotide-binding-leucine-rich repeat genes. Genetics, 181, 1627-1638.
28. 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.
29. Librado, P., and, Rozas, J., (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
30. Liu, X., Lin, F., Wang, L., and, Pan, Q., (2007) The in silico map-based cloning of Pi36, a rice coiled-coil-nucleotide-binding site-leucine-rich repeat gene that confers race-specific resistance to the blast fungus. Genetics, 176, 2541-2549. (Pubitemid 47360681)
31. 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. 11, 419-427.
32. Loutre, C., Wicker, T., Travella, S., Galli, P., Scofield, S., Fahima, T., Feuillet, C., and, Keller, B., (2009) Two different CC-NBS-LRR genes are required for Lr10-mediated leaf rust resistance in tetraploid and hexaploid wheat. Plant. J. 60, 1043-1054.
33. Meyers, B.C., Kaushik, S., and, Nandety, R.S., (2005) Evolving disease resistance genes. Curr. Opin. Plant Biol. 8, 129-134. (Pubitemid 40323540)
34. Miki, S., Matsui, K., Kito, H., 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.
35. Narusaka, M., Shirasu, K., Noutoshi, Y., Kubo, Y., Shiraishi, T., Iwabuchi, M., and, Narusaka, Y., (2009) RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J. 60, 218-226.
36. Nei, M., (1987) Molecular Evolutionary Genetics. New York, NY: Columbia University Press.
37. 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. (Pubitemid 32053392)
38. Rakshit, S., Kanzaki, H., Matsumura, H., et al. (2010) Use of TILLING for reverse and forward genetics of rice. In The Handbook of Plant Mutation Screening: Mining of Natural and Induced Alleles (, Meksem, K., and, Kahl, G., eds). Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA, pp. 187-197.
39. 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.
40. Swofford, D.L., (2003) PAUP. Phylogenetic Analysis Using Parsimony (and Other Methods). Version 4, Sunderland, Massachusetts: Sinauer Associates.
41. Tajima, F., (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595. (Pubitemid 19274682)
42. Takehisa, H., Yasuda, M., Fukuta, Y., Kobayashi, N., Hayashi, N., Nakashita, H., Abe, T., and, Sato, T., (2009) Genetic analysis of resistance genes in an Indica-type rice (Oryza sativa L.), Kasalath, using DNA markers. Breed. Sci. 59, 253-260.
43. Terauchi, R., and, Yoshida, K., (2010) Towards population genomics of effector-effector target interactions. New Phytol. 187, 929-939.
44. Toki, S., Hara, N., Ono, K., Onodera, H., Tagiri, A., Oka, S., and, Tanaka, H., (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J. 47, 969-976. (Pubitemid 44326445)
45. Wang, Z., Teramino, G., Yang, D., Liu, G., Tingrey, S.V., Miao, G.-H., and, Wang, G.-L., (2001) Rice ESTs with disease-resistance gene- or defense-response gene-like sequences mapped to regions containing major resistance genes or QTLs. Mol. Genet. Genomics, 265, 302-310.
46. Wei, F., Gobelman-Werner, K., Morroll, S.M., Kurth, J., Mao, L., Wing, R., Leister, D., Schulze-Lefert, P., and, Wise, R.P., (1999) The Mla (powdery mildew) resistance cluster is associated with three NBS-LRR gene families and suppressed recombination within a 240-kb DNA interval on chromosome 5S (1HS) of barley. Genetics, 153, 1929-1948.
47. 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. (Pubitemid 35435167)
48. Xu, J.-R., Peng, Y.-L., Dickman, M.B., and, Sharon, A., (2006) The dawn of fungal pathogen genomics. Annu. Rev. Phytopathol. 44, 337-366. (Pubitemid 44435708)
49. Yang, Z., (2007) PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol. Biol. Evol. 24, 1586-1591. (Pubitemid 47236688)
50. 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.
51. Yu, J., Hu, S., Wang, J., et al. (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science, 296, 79-92. (Pubitemid 34280064)
52. Zeigler, R.S., Leong, S.A., and, Teng, P.S., (1994) Rice Blast Disease. Los Banos, Laguna, Philippines: CAB International Rice Research Institute.
53. Zhou, T., Wang, Y., Chen, J.-Q., Araki, H., Jing, Z., Jiang, K., Shen, J., and, Tian, D., (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol. Genet. Genomics, 271, 402-415. (Pubitemid 38824034)
54. Zhou, B., Qu, S., Liu, G., Dolan, M., Sakai, H., Lu, G., Bellizzi, M., and, Wang, G.L., (2006) The eight amino-acid differences within three leucine-rich repeats between Pi2 and Piz-t resistance proteins determine the resistance specificity to Magnaporthe grisea. Mol. Plant-Microbe Interact. 19, 1216-1228. (Pubitemid 44607333)