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Genomic structure and evolution of the Pi2/9 locus in wild rice species

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Abstract

Rice blast, caused by the fungal pathogen Magnaporthe oryzae, is a devastating disease of rice worldwide. Among the 85 mapped resistance (R) genes against blast, 13 have been cloned and characterized. However, how these genes originated and how they evolved in the Oryza genus remains unclear. We previously cloned the rice blast R-genes Pi2, Pi9, and Piz-t, and analyzed their genomic structure and evolution in cultivated rice. In this study, we determined the genomic sequences of the Pi2/9 locus in four wild Oryza species representing three genomes (AA, BB and CC). The number of Pi2/9 family members in the four wild species ranges from two copies to 12 copies. Although these genes are conserved in structure and categorized into the same subfamily, sequence duplications and subsequent inversions or uneven crossing overs were observed, suggesting that the locus in different wild species has undergone dynamic changes. Positive selection was found in the leucine-rich repeat region of most members, especially in the largest clade where Pi9 is included. We also provide evidence that the Pi9 gene is more related to its homologues in the recurrent line and other rice cultivars than to those in its alleged donor species O. minuta, indicating a possible origin of the Pi9 gene from O. sativa. Comparative sequence analysis between the four wild Oryza species and the previously established reference sequences in cultivated rice species at the Pi2/9 locus has provided extensive and unique information on the genomic structure and evolution of a complex R-gene cluster in the Oryza genus.

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References

  • Amante-Bordeos A, Sitch LA, Nelson R, Damacio RD, Oliva L, Aswidinnoor H, Leung H (1992) Transfer of bacterial blight and blast resistance from the tetraploid wild rice Oryza minuta to cultivated rice, Oryza sativa. Theor Appl Genet 84:345–354

    Article  Google Scholar 

  • Ameline-Torregrosa CB, Wang B, O’Bleness MS, Deshpande S, Zhu H, Roe B, Young ND, Cannon SB (2008) Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiol 146:5–21

    Article  PubMed  CAS  Google Scholar 

  • Ammiraju JSS, Lu F, Sanyal A, Yu Y, Song X, Jiang J, Pontaroli AC, Rambo T, Currie J, Collura K, Talag J, Fan C, Goicoechea JL, Zuccolo A, Chen J, Bennetzen JL, Chen M, Jackson S, Wing RA (2008) Dynamic evolution of Oryza genomes is revealed by comparative genomic analysis of a genus-wide vertical data set. Plant Cell 20:3191–3209

    Article  PubMed  CAS  Google Scholar 

  • Bai JL, Pennill A, Ning J, Lee SW, Ramalingam J, Webb CA, Zhao B, Sun Q, Nelson JC, Leach JE, Hulbert SH (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12:1871–1884

    Article  PubMed  CAS  Google Scholar 

  • Ballini E, Morel JB, Droc G, Price A, Courtois B, Notteghem JL, Tharreau D (2008) A genome-wide meta-analysis of rice blast resistance genes and quantitative trait loci provides new insights into partial and complete resistance. Mol Plant Microbe Interact 21:859–868

    Article  PubMed  CAS  Google Scholar 

  • Caracuel-Rios Z, Talbot NJ (2007) Cellular differentiation and host invasion by the rice blast fungus Magnaporthe grisea. Curr Opin Microbiol 10:339–345

    Article  PubMed  CAS  Google Scholar 

  • Dodds PN, Lawrence GJ, Ellis JG (2001) Six amino acid changes confined to the leucine-rich repeat β-strand/β-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell 13:163–178

    Article  PubMed  CAS  Google Scholar 

  • Ellis JG, Lawrence GJ, Luck JE, Dodds PN (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

    Article  PubMed  CAS  Google Scholar 

  • Ewing B, Green P (1998) Base calling of automated sequencer traces using Phred II. Error probabilities. Genome Res 8:186–194

    PubMed  CAS  Google Scholar 

  • Ewing B, Hillier L, Wendl M, Green P (1998) Base calling of automated sequencer traces using Phred I. Accuracy assessment. Genome Res 8:175–185

    PubMed  CAS  Google Scholar 

  • Fukuoka S, Saka N, Koga H, Ono K, Shimizu T, Ebana K, Hayashi N, Takahashi H, Hirochika A, Okuno K, Yano M (2009) Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325:998–1001

    Article  PubMed  CAS  Google Scholar 

  • Geffroy V, Macadre C, David P, Pedrosa-Harand A, Sevignac M, Dauga C, Langin T (2009) Molecular analysis of a large subtelomeric nucleotide-binding-site-leucine-rich-repeat family in two representative genotypes of the major gene pools of Phaseolus vulgaris. Genetics 181:405–419

    Article  PubMed  CAS  Google Scholar 

  • Gordon D, Abajian C, Green P (1998) Consed, a graphical tool for sequence finishing. Genome Res 8:195–202

    PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Series 41:95–98

    CAS  Google Scholar 

  • Hichey DA, Bally-Cuif L, Abukashawa S, Payant V, Benkel BF (1991) Concerted evolution of duplicated protein-coding genes in Drosophila. Proc Natl Acad Sci USA 88:1611–1615

    Article  Google Scholar 

  • Huang CL, Hwang SY, Chiang YC, Lin TP (2008) Molecular evolution of the Pi-ta gene resistant to rice blast in wild rice (Oryza rufipogon). Genetics 179:1527–1538

    Article  PubMed  CAS  Google Scholar 

  • Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312

    Article  PubMed  CAS  Google Scholar 

  • Kruijt M, Brandwagt BF, De Wit PJGM (2004) Rearrangements in the Cf-9 disease resistance gene cluster of wild tomato have resulted in three genes that mediate Avr9 responsiveness. Genetics 168:1655–1663

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Costanzo S, Jia Y, Olsen KM, Caicedo AL (2009) Evolutionary dynamics of the genomic region around the blast resistance gene Pi-ta in AA genome Oryza Species. Genetics 183:1315–1325

    Article  PubMed  CAS  Google Scholar 

  • Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet 20:116–122

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Liu X, Dai L, Wang G (2007) Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. J Genet Genomics 34:765–776

    Article  PubMed  Google Scholar 

  • Lu F, Ammiraju JS, Sanyal A, Zhang S, Song R, Chen J, Li G, Sui Y, Song X, Cheng Z, de Oliveira AC, Bennetzen JL, Jackson SA, Wing RA, Chen M (2009) Comparative sequence analysis of MONOCULM1-orthologous regions in 14 Oryza genomes. Proc Natl Acad Sci USA 106:2071–2076

    Article  PubMed  CAS  Google Scholar 

  • Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci USA 101:12404–12410

    Article  PubMed  CAS  Google Scholar 

  • Maricio R, Stahl EA, Korves T (2003) Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana. Genetics 163:735–746

    Google Scholar 

  • Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23–61

    Article  PubMed  CAS  Google Scholar 

  • McDowell JM, Dhandaydham M, Long TA, Aarts MG, Goff S, Holub EB, Dangl JL (1998) Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 10:1861–1874

    Article  PubMed  CAS  Google Scholar 

  • McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212

    Article  PubMed  Google Scholar 

  • Meyers BC, Chin DB, Shen KA, Sivaramakrishnan S, Lavelle DO, Zhang Z, Michelmore RW (1998a) The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10:1817–1832

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Shen KA, Rohani P, Gaut BS, Michelmore RW (1998b) Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 10:1833–1846

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834

    Article  PubMed  CAS  Google Scholar 

  • Monosi B, Wisser RJ, Pennill L, Hulbert SH (2004) Full-genome analysis of resistance gene homologues in rice. Theor Appl Genet 109:1434–1447

    Article  PubMed  CAS  Google Scholar 

  • Noel L, Moores TL, Van der Biezen EA, Parniske M, Daniels MJ, Parker JE, Jones JD (1999) Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 11:2099–2111

    Article  PubMed  CAS  Google Scholar 

  • Parniske M, Jones JD (1999) Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family. Proc Natl Acad Sci USA 96:5850–5855

    Article  PubMed  CAS  Google Scholar 

  • Perriere G, Gouy M (1996) WWW-Query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369

    Article  PubMed  CAS  Google Scholar 

  • Qu S, Liu G, Zhou B, Bellizzi M, Zeng L, Dai L, Han H, Wang GL (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

    Article  PubMed  CAS  Google Scholar 

  • Shang J, Tao Y, Chen X, Zou Y, Lei C, Wang J, Li X, Zhao X, Zhang M, Lu Z, Xu J, Cheng Z, Wan J, Zhu L (2009) Identification of a new rice blast resistance gene, Pid3, by genomewide comparison of paired nucleotide-binding site-leucine-rich repeat genes and their pseudogene alleles between the two sequenced rice genomes. Genetics 182:1303–1311

    Article  PubMed  CAS  Google Scholar 

  • Shimamoto K, Kyozuka J (2002) Rice as a model for comparative genomics of plants. Annu Rev Plant Biol 53:399–419

    Article  PubMed  CAS  Google Scholar 

  • Song WY, Pi LY, Wang GL, Gardner J, Holsten T, Ronald P (1997) Evolution of the rice Xa21 disease resistance gene family. Plant Cell 9:1279–1287

    Article  PubMed  CAS  Google Scholar 

  • Sun Q, Collins NC, Ayliffe M, Smith SM, Drake J, Pryor T, Hulbert SH (2001) Recombination between paralogues at the rp1 rust resistance locus in maize. Genetics 158:423–438

    PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Valent B (1990) Rice blast as a model system for plant pathology. Phytopathology 80:33–36

    Article  Google Scholar 

  • Vitte C, Panaud O (2003) Formation of solo-LTRs through unequal homologous recombination counterbalances amplifications of LTR retrotransposons in rice Oryza sativa L. Mol Biol Evol 20:528–540

    Article  PubMed  CAS  Google Scholar 

  • Walsh JB (1987) Sequence-dependent gene conversion: can duplicated genes diverge fast enough to escape conversion? Genetics 117:543–557

    PubMed  CAS  Google Scholar 

  • Wang X, Jia Y, Shu QY, Wu D (2008) Haplotype diversity at the Pi-ta locus in cultivated rice and its wild relatives. Phytopathology 98:1305–1311

    Article  PubMed  CAS  Google Scholar 

  • Webb CA, Richter TE, Collins NC, Nicolas M, Trick HN, Pryor T, Hulbert SH (2002) Genetic and molecular characterization of the maize rp3 rust resistance locus. Genetics 162:381–394

    PubMed  CAS  Google Scholar 

  • Wei F, Wing RA, Roger PW (2002) Genome dynamics and evolution of the Mla (Powdery mildew) resistance locus in barley. Plant Cell 14:1903–1917

    Article  PubMed  CAS  Google Scholar 

  • Wicker T, Yahiaoui N, Keller B (2007) Contrasting rates of evolution in Pm3 loci from three wheat species and rice. Genetics 177:1207–1216

    Article  PubMed  CAS  Google Scholar 

  • Wing RA, Ammiraju JS, Luo M, Kim H, Yu Y, Kudrna D, Zuccolo A, Ammiraju JS, Luo M, Nelson W, Ma J, SanMiguel P, Hurwitz B, Ware D, Brar D, Mackill D, Soderlund C, Stein L, Jackson S (2005) The oryza map alignment project: the golden path to unlocking the genetic potential of wild rice species. Plant Mol Biol 59:53–62

    Article  PubMed  CAS  Google Scholar 

  • Wisser RJ, Qi S, Hulbert SH, Kresovich S, Nelson RJ (2005) Identification and characterization of regions of the rice genome associated with broad-spectrum, quantitative disease resistance. Genetics 169:2277–2293

    Article  PubMed  CAS  Google Scholar 

  • Xiao S, Emerson B, Ratanasut K, Patrick E, O’Neill C, Bancroft I, Turner JG (2004) Origin and maintenance of a broad-spectrum disease resistance locus in Arabidopsis. Mol Biol Evol 21:1661–1672

    Article  PubMed  CAS  Google Scholar 

  • Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556

    PubMed  CAS  Google Scholar 

  • Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449

    PubMed  CAS  Google Scholar 

  • Yoshida K, Miyashita NT (2009) DNA polymorphism in the blast disease resistance gene Pita of the wild rice Oryza rufipogon and its related species. Genes Genet Syst 84(2):121–136

    Article  PubMed  CAS  Google Scholar 

  • Zhou B, Qu S, Liu G, Dolan M, Sakai H, Lu G, Bellizzi M, Wang GL (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

    Article  PubMed  CAS  Google Scholar 

  • Zhou B, Dolan M, Sakai H, Wang GL (2007) The genomic dynamics and evolutionary mechanism of the Pi2/9 locus in rice. Mol Plant Microbe Interact 20:63–71

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This project was supported by the “973” Project (2006CB101904), the “948” Project (2006-G61), the Henye Project of Ministry of Agriculture, National Natural Science Foundation of China (30828022), and the NSF-Plant Genome Research Program (#0605017).

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Authors and Affiliations

  1. Hunan Provincial Key Laboratory of Crop Germplasm Innovation and Utilization, Hunan Agricultural University, Changsha, 410128, China

    Liangying Dai, Jun Wu, Xuejun Wang, Xionglun Liu & Guo-Liang Wang

  2. National Center For Gene Research, Chinese Academy of Sciences, Shanghai, 200233, China

    Jun Wu, Xunbo Li, Bin Han & Bo Zhou

  3. Department of Plant Pathology, Ohio State University, Columbus, OH, 43210, USA

    Chatchawan Jantasuriyarat & Guo-Liang Wang

  4. Institute of Biotechnology, Zhejiang University, Hangzhou, 310029, China

    Bo Zhou

  5. Arizona Genomics Institute, School of Plant Sciences and BIO5 Institute for Collaborative Research, University of Arizona, Tucson, AZ, 85721, USA

    Dave Kudrna, Yeisoo Yu & Rod A. Wing

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  1. Liangying Dai
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  2. Jun Wu
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  3. Xunbo Li
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  4. Xuejun Wang
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  8. Yeisoo Yu
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  9. Rod A. Wing
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  10. Bin Han
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  11. Bo Zhou
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  12. Guo-Liang Wang
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Corresponding authors

Correspondence to Bo Zhou or Guo-Liang Wang.

Additional information

Communicated by E. Guiderdoni.

L. Dai and J. Wu contributed equally to this work.

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Dai, L., Wu, J., Li, X. et al. Genomic structure and evolution of the Pi2/9 locus in wild rice species. Theor Appl Genet 121, 295–309 (2010). https://doi.org/10.1007/s00122-010-1310-0

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