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

Plant resistance genes (R genes) harbor tremendous allelic diversity, constituting a robust immune system effective against microbial pathogens. Nevertheless, few functional R genes have been identified for even the best-studied pathosystems. Does this limited repertoire reflect specificity, with most R genes having been defeated by former pests, or do plants harbor a rich diversity of functional R genes, the composite behavior of which is yet to be characterized? Here, we survey 332 NBS-LRR genes cloned from five resistant Oryza sativa (rice) cultivars for their ability to confer recognition of 12 rice blast isolates when transformed into susceptible cultivars. Our survey reveals that 48.5% of the 132 NBS-LRR loci tested contain functional rice blast R genes, with most R genes deriving from multi-copy clades containing especially diversified loci. Each R gene recognized, on average, 2.42 of the 12 isolates screened. The abundant R genes identified in resistant genomes provide extraordinary redundancy in the ability of host genotypes to recognize particular isolates. If the same is true for other pathogens, many extant NBS-LRR genes retain functionality. Our success at identifying rice blast R genes also validates a highly efficient cloning and screening strategy.

[1]  L. Hurst,et al.  Parent–progeny sequencing indicates higher mutation rates in heterozygotes , 2015, Nature.

[2]  B C Meyers,et al.  Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. , 1998, Genome research.

[3]  E. Stahl,et al.  Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis , 1999, Nature.

[4]  Sihai Yang,et al.  Rapid evolution of avirulence genes in rice blast fungus Magnaporthe oryzae , 2014, BMC Genetics.

[5]  B. Han,et al.  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 , 2006, Genetics.

[6]  E. Stahl,et al.  Evolutionary Dynamics of Plant R-Genes , 2001, Science.

[7]  J. Bergelson,et al.  Reduced Genetic Variation Occurs among Genes of the Highly Clonal Plant Pathogen Xanthomonas axonopodis pv. vesicatoria, Including the Effector Gene avrBs2 , 2005, Applied and Environmental Microbiology.

[8]  H. Yoshida,et al.  Refunctionalization of the ancient rice blast disease resistance gene Pit by the recruitment of a retrotransposon as a promoter. , 2009, The Plant journal : for cell and molecular biology.

[9]  S. Bhattacharjee,et al.  Effector-triggered immunity signaling: from gene-for-gene pathways to protein-protein interaction networks. , 2012, Molecular plant-microbe interactions : MPMI.

[10]  H H Flor,et al.  Current Status of the Gene-For-Gene Concept , 1971 .

[11]  G. Martin,et al.  Deletions in the Repertoire of Pseudomonas syringae pv. tomato DC3000 Type III Secretion Effector Genes Reveal Functional Overlap among Effectors , 2009, PLoS pathogens.

[12]  R. Innes.  Genetic dissection of R gene signal transduction pathways. , 1998, Current opinion in plant biology.

[13]  A. America,et al.  Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode , 2012, Proceedings of the National Academy of Sciences.

[14]  Jian-Qun Chen,et al.  Genome-wide investigation on the genetic variations of rice disease resistance genes , 2006, Plant Molecular Biology.

[15]  Guo-Liang Wang,et al.  Recent progress and understanding of the molecular mechanisms of the rice-Magnaporthe oryzae interaction. , 2010, Molecular plant pathology.

[16]  D. K. Willis,et al.  Copy Number Variation of Multiple Genes at Rhg1 Mediates Nematode Resistance in Soybean , 2012, Science.

[17]  Dacheng Tian,et al.  Widely distributed hot and cold spots in meiotic recombination as shown by the sequencing of rice F2 plants. , 2015, The New phytologist.

[18]  D. Hartl,et al.  Rapidly evolving R genes in diverse grass species confer resistance to rice blast disease , 2013, Proceedings of the National Academy of Sciences.

[19]  L. Dai,et al.  Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. , 2007, Journal of genetics and genomics = Yi chuan xue bao.

[20]  B. Staskawicz,et al.  Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[21]  B. McDonald,et al.  Pathogen population genetics, evolutionary potential, and durable resistance. , 2002, Annual review of phytopathology.

[22]  I. Ashikawa,et al.  Development of PCR-based SNP markers for rice blast resistance genes at the Piz locus , 2004, Theoretical and Applied Genetics.

[23]  J. Bonman,et al.  Physiologic Specialization of Pyricularia oryzae in the Philippines , 1986 .

[24]  J. Bergelson,et al.  Effector genes of Xanthomonas axonopodis pv. vesicatoria promote transmission and enhance other fitness traits in the field. , 2004, Genetics.

[25]  Xinqiong Liu,et al.  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 , 2007, Genetics.

[26]  Xinli Sun,et al.  Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. , 2004, The Plant journal : for cell and molecular biology.

[27]  Q. Sun,et al.  Resistance gene complexes: evolution and utilization. , 2001, Annual review of phytopathology.

[28]  B. Valent,et al.  Recent advances in rice blast effector research. , 2010, Current opinion in plant biology.

[29]  R. Michelmore,et al.  Impacts of resistance gene genetics, function, and evolution on a durable future. , 2013, Annual review of phytopathology.

[30]  M. Kreitman,et al.  A Genome-Wide Survey of R Gene Polymorphisms in Arabidopsis[W] , 2006, The Plant Cell Online.

[31]  R. Terauchi,et al.  The Rice Resistance Protein Pair RGA4/RGA5 Recognizes the Magnaporthe oryzae Effectors AVR-Pia and AVR1-CO39 by Direct Binding[W][OA] , 2013, Plant Cell.

[32]  H. Leung,et al.  Genetic control of rice blast resistance in the durably resistant cultivar Gumei 2 against multiple isolates , 2005, Theoretical and Applied Genetics.

[33]  B. Meyers,et al.  Tracing the origin and evolutionary history of plant nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes. , 2012, The New phytologist.

[34]  M. S. Mukhtar,et al.  Independently Evolved Virulence Effectors Converge onto Hubs in a Plant Immune System Network , 2011, Science.

[35]  M. Rep,et al.  Suppression of Plant Resistance Gene-Based Immunity by a Fungal Effector , 2008, PLoS pathogens.

[36]  Blake C Meyers,et al.  Multiple Genetic Processes Result in Heterogeneous Rates of Evolution within the Major Cluster Disease Resistance Genes in Lettucew⃞ , 2004, The Plant Cell Online.

[37]  O. Edelbaum,et al.  Tobacco Mosaic Virus Regulates the Expression of Its Own Resistance Gene N1 , 2004, Plant Physiology.

[38]  P. R. Jennings,et al.  Progress in the Development of Disease-Resistant Rice , 1969 .

[39]  R. Terauchi,et al.  Multiple Translocation of the AVR-Pita Effector Gene among Chromosomes of the Rice Blast Fungus Magnaporthe oryzae and Related Species , 2011, PLoS pathogens.