A genome-wide survey reveals abundant rice blast R genes in resistant cultivars

Plant Journal

Volumn 84, Issue 1, 2015, Pages 20-28

  Zhang, Xiaohui ^a   Yang, Sihai ^a   Wang, Jiao ^a   Jia, Yanxiao ^a   Huang, Ju ^a   Tan, Shengjun ^a   Zhong, Yan ^a   Wang, Ling ^b   Gu, Longjiang ^a   Chen, Jian Qun ^a   Pan, Qinghua ^b   Bergelson, Joy ^c   Tian, Dacheng ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

genome wide survey; Magnaporthe oryzae; Oryza sativa; plant resistance genes; rice blast

Indexed keywords

BLAST RESISTANCE; CLONE CELLS; CLONING; PLANTS (BOTANY); SURVEYS;

COMPOSITE BEHAVIOR; MAGNAPORTHE ORYZAE; MICROBIAL PATHOGENS; ORYZA SATIVA; PLANT RESISTANCE GENES; RESISTANT CULTIVARS; RICE BLASTS; SCREENING STRATEGY;

GENES;

PLANT PROTEIN;

DISEASE RESISTANCE; DNA SEQUENCE; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MAGNAPORTHE; MICROBIOLOGY; ORYZA; PHYSIOLOGY;

DISEASE RESISTANCE; GENOME-WIDE ASSOCIATION STUDY; MAGNAPORTHE; ORYZA; PLANT PROTEINS; SEQUENCE ANALYSIS, DNA;

EID: 84942789055     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12955     Document Type: Article

References (44)

1. Bakker, E.G., Toomajian, C., Kreitman, M., and, Bergelson, J., (2006) A Genome-Wide Survey of R Gene Polymorphisms in Arabidopsis. Plant Cell, 18, 1803-1818.
2. Bergelson, J., Kreitman, M., Stahl, E.A., and, Tian, D., (2001) Evolutionary dynamics of plant R-genes. Science, 292, 2281-2285.
3. Bonman, J.M., Dedios, T.V., and, Khin, M.M., (1986) Physiologic specialization of Pyricularia oryzae in the Philippines. Plant Dis. 70, 767-769.
4. Cesari, S., Thilliez, G., Ribot, C., et al. (2013) The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell, 25, 1463-1481.
5. Chuma, I., Isobe, C., Hotta, Y., 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.
6. Cook, D.E., Lee, T.G., Guo, X., et al. (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science, 338, 1206-1209.
7. Flor, H.H., (1971) Current status of gene-for-gene concept. Annu. Rev. Phytopathol. 9, 275-296.
8. Gassmann, W., and, Bhattacharjee, S., (2012) Effector-triggered immunity signaling: from gene-for-gene pathways to protein-protein interaction networks. Mol. Plant-Microbe Interact. 25, 862-868.
9. Hayashi, K., and, Yoshida, H., (2009) Refunctionalization of the ancient rice blast disease resistance gene Pit by the recruitment of a retrotransposon as a promoter. Plant J. 57, 413-425.
10. Hayashi, K., Hashimoto, N., Daigen, M., and, Ashikawa, I., (2004) Development of PCR-based SNP markers for rice blast resistance genes at the Piz locus. Theor. Appl. Genet. 108, 1212-1220.
11. Houterman, P.M., Cornelissen, B.J.C., and, Rep, M., (2008) Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathog. 4, e1000061.
12. Huang, J., Si, W., Deng, Q., Li, P., and, Yang, S., (2014) Rapid evolution of avirulence genes in rice blast fungus Magnaporthe oryzae. BMC Genet. 15, 45.
13. Hulbert, S.H., Webb, C.A., Smith, S.M., and, Sun, Q., (2001) Resistance gene complexes: evolution and utilization. Annu. Rev. Phytopathol. 39, 285-312.
14. Innes, R.W., (1998) Genetic dissection of R gene signal transduction pathways. Curr. Opin. Plant Biol. 1, 299-304.
15. Kitamura, S.C.E., (1954) Breeding of blast resistant varieties by hybridization between japonica and indica paddy rices [in Japanese]. J. Agric. Sci. 9, 321-323.
16. Kuang, H., Woo, S.-S., Meyers, B.C., Nevo, E., and, Michelmore, R.W., (2004) Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell, 16, 2870-2894.
17. Kvitko, B.H., Park, D.H., Velásquez, A.C., Wei, C.-F., Russell, A.B., Martin, G.B., Schneider, D.J., and, Collmer, A., (2009) Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathog. 5, e1000388.
18. Levy, M., Edelbaum, O., and, Sela, I., (2004) Tobacco mosaic virus regulates the expression of its own resistance gene N. Plant Physiol. 135, 2392-2397.
19. Lin, S., and, Min, S., (1991) Rice Varieties and Their Genealogy in China. Shanghai, China: Shanghai Sci. Technol Press, 414.
20. Lin, F., Chen, S., Que, Z., Wang, L., Liu, X., and, Pan, Q., (2007) The blast resistance gene Pi37 encodes a nucleotide binding site leucine-rich repeat protein and is a member of a resistance gene cluster on rice chromosome 1. Genetics, 177, 1871-1880.
21. Liu, J., Liu, X., Dai, L., and, Wang, G., (2007) Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. J. Genet. Genomics, 34, 765-776.
22. 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.
23. Lozano-Torres, J.L., Wilbers, R.H.P., Gawronski, P., et al. (2012) Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode. Proc. Natl Acad. Sci. USA, 109, 10119-10124.
24. Mach, J., (2013) The direct approach: resistance genes team up to recognize different fungal effectors in rice. Plant Cell, 25, 1189.
25. McDonald, B.A., and, Linde, C., (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40, 349-379.
26. Michelmore, R.W., and, Meyers, B.C., (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8, 1113-1130.
27. Michelmore, R.W., Christopoulou, M., and, Caldwell, K.S., (2013) Impacts of resistance gene genetics, function, and evolution on a durable future. Annu. Rev. Phytopathol. 51, 291-319.
28. Mukhtar, M.S., Carvunis, A.-R., Dreze, M., et al. (2011) Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science, 333, 596-601.
29. Ou, S.H., and, Jennings, P.R., (1969) Progress in the development of disease-resistant rice. Annu. Rev. Phytopathol. 7, 383-410.
30. Peng, S., Huang, F.Y., Sun, G.C., Liu, E.M., Sun, Y.J., Ai, R.X., Zhao, J.X., Bai, S.Z., and, Xiao, F.H., (1996) Studies on durable resistance to blast disease in different latitudes for rice. Sci. Agric. Sin. 29, 52-58.
31. Qu, S., Liu, G., Zhou, B., Bellizzi, M., Zeng, L., Dai, L., Han, B., and, Wang, G.L., (2006) The broad-spectrum blast resistance gene Pi9 encodes a nucleotide-binding site-leucine-rich repeat protein and is a member of a multigene family in rice. Genetics, 172, 1901-1914.
32. Si, W., Yuan, Y., Huang, J., et al. (2015) Widely distributed hot and cold spots in meiotic recombination as shown by the sequencing of rice F2 plants. New Phytol. 206, 1491-1502.
33. Spielmeyer, W., Mago, R., Wellings, C., and, Ayliffe, M., (2013) Lr67 and Lr34 rust resistance genes have much in common-they confer broad spectrum resistance to multiple pathogens in wheat. BMC Plant Biol. 13, 96.
34. 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.
35. Sun, X., Cao, Y., Yang, Z., Xu, C., Li, X., Wang, S., and, Zhang, Q., (2004) Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J. 37, 517-527.
36. Tai, T.H., Dahlbeck, D., Clark, E.T., Gajiwala, P., Pasion, R., Whalen, M.C., Stall, R.E., and, Staskawicz, B.J., (1999) Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc. Natl Acad. Sci. USA, 96, 14153-14158.
37. Valent, B., and, Khang, C.H., (2010) Recent advances in rice blast effector research. Curr. Opin. Plant Biol. 13, 434-441.
38. Wichmann, G., and, Bergelson, J., (2004) Effector genes of Xanthomonas axonopodis pv. vesicatoria promote transmission and enhance other fitness traits in the field. Genetics, 166, 693-706.
39. Wichmann, G., Ritchie, D., Kousik, C.S., and, Bergelson, J., (2005) Reduced genetic variation occurs among genes of the highly clonal plant pathogen Xanthomonas axonopodis pv. vesicatoria, including the effector gene avrBs2. Appl. Environ. Microbiol. 71, 2418-2432.
40. Wu, J.-L., Fan, Y.-Y., Li, D.-B., Zheng, K.-L., Leung, H., and, Zhuang, J.-Y., (2005) Genetic control of rice blast resistance in the durably resistant cultivar Gumei 2 against multiple isolates. Theor. Appl. Genet. 111, 50-56.
41. Yang, S., Feng, Z., Zhang, X., Jiang, K., Jin, X., Hang, Y., Chen, J.Q., and, Tian, D., (2006) Genome-wide investigation on the genetic variations of rice disease resistance genes. Plant Mol. Biol. 62, 181-193.
42. Yang, S., Li, J., Zhang, X., Zhang, Q., Huang, J., Chen, J.-Q., Hartl, D.L., and, Tian, D., (2013) Rapidly evolving R genes in diverse grass species confer resistance to rice blast disease. Proc. Natl Acad. Sci. USA 110, 18572-18577.
43. Yang, S., Wang, L., Huang, J., Zhang, X., Yuan, Y., Chen, J.-Q., Hurst, L.D., and, Tian, D., (2015) Parent-progeny sequencing indicates higher mutation rates in heterozygotes. Nature, 523, 463-467.
44. Yue, J.X., Meyers, B.C., Chen, J.Q., Tian, D., and, Yang, S., (2012) Tracing the origin and evolutionary history of plant nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes. New Phytol. 193, 1049-1063.