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Molecular diversity in rice blast resistance gene Pi-ta makes it highly effective against dynamic population of Magnaporthe oryzae

Functional & Integrative Genomics volume 13, pages 309–322 (2013)Cite this article

Abstract

Rice blast is one of the important diseases of rice which can be effectively managed by the deployment of resistance genes. Pi-ta is one of the major blast resistant genes effective against pathogen populations in different parts of India. We analysed allelic variants of Pi-ta from 48 rice lines selected after phenotyping of 529 rice landraces across three eco-geographical blast hot spot regions. Besides, Pi-ta orthologue sequences of 220 rice accessions belonging to wild and cultivated species of rice were also included in the study for a better evo–devo perspective of the diversity present in the gene and the selection pressures acting on this locus. We obtained high nucleotide variations (SNPs and insertion–deletions) in the intronic region. We also identified 64 haplotypes based on nucleotide polymorphism in these alleles. Pi-ta orthologues of Indian landraces were scattered in eight major haplotypes indicating its heterogenous nature. We identified a total of 47 different Pi-ta protein variants on the basis of deduced amino acid residues amongst the orthologues. Five unique and novel Pi-ta variants were identified for the first time in rice landraces exhibiting different reaction types against the Magnaporthe oryzae population. A high value of Pinon/syn was observed only in the leucine-rich domain of the alleles cloned from Indian landraces, indicating strong selective forces acting on this region. The detailed molecular analysis of the Pi-ta orthologues provides insights to a high degree of inter- and intraspecific relationships amongst the Oryza species. We identified rice landraces possessing the effective alleles of this resistance gene which can be used in future blast resistance breeding programmes.

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References

  • Ashikawa I, Wu J, Matsumoto T, Ishikawa R (2009) Haplotype diversity and molecular evolution of the rice Pikm locus for blast resistance. J Gen Plant Pathol 1–6

  • Bakker EG, Toomajian C, Kreitman C, Bergelson J (2006) A genome-wide survey of R- gene polymorphisms in Arabidopsis. Plant Cell 18:1803–1818

    PubMed  Article  CAS  Google Scholar 

  • Bonmann JM, Dedios TV, Khin MM (1986) Physiologic specialization 718 of Pyricularia oryzae in Philippines. Plant Dis 70:767–769

    Article  Google Scholar 

  • Bryan GT, Wu KS, Farrall L, Jia Y, Hershey HP, McAdams SA, Faulk KN, Donaldson GK, Tarchini R, Valent B (2000) tA single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell 12(11):2033–2046

    PubMed  CAS  Google Scholar 

  • Dai Y, Jia Y, Correll J, Wang X, Wang Y (2010) Diversification and evolution of the avirulence gene AVR-Pita1 in fields isolate of Magnaporthe oryzae. Fungal Genet Biol 47:973–980

    PubMed  Article  CAS  Google Scholar 

  • Das A, Soubam D, Singh PK, Thakur S, Singh NK, Sharma TR (2012) A novel blast resistance gene, Pi54rh cloned from wild species of rice, Oryza rhizomatis confers broad spectrum resistance to Magnaporthe oryzae. Funct Integr Genomics 12:215–228

    PubMed  Article  CAS  Google Scholar 

  • Ewing B, Green P (1985) Base calling sequencer traces using Phred II. Error probabilities. Genome Res 8(3):175–185

    Article  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver 30: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50

    CAS  Google Scholar 

  • Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    PubMed  CAS  Google Scholar 

  • Gupta PK, Rustogi S (2004) Molecular markers from the transcribed/expressed region of the genome in higher plants. Funct Integr Genomics 4:139–162

    PubMed  Article  CAS  Google Scholar 

  • Hwang CF, Bhakta AV, Truesdell GM, Pudlo WM, Williamson VM (2000) Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell 12:1319–1329

    PubMed  CAS  Google Scholar 

  • Huang E, Hwang S, Chiang Y, lin T (2008) Molecular evolution of the Pi-ta gene resistant to rice blast in wild rice (Oryza rufipogon). Genetics 179:1527–1538

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • IRGSP (International Rice Genome Sequencing Project) (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  Google Scholar 

  • Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19:4004–4014

    PubMed  Article  CAS  Google Scholar 

  • Jia Y, Martin R (2008) Identification of a new locus Ptr(t) required for rice blast resistance gene Pi-ta-mediated resistance. Mol Plant Microbe Interact 21:396–403

    PubMed  Article  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

    PubMed  Article  CAS  Google Scholar 

  • Lee S, Jia Y, Jia M, Gealy DR, Olsen KM (2011) Molecular evolution of the rice blast resistance gene Pi-ta in invasive weedy rice in the USA. PLoS ONE 6(10):e26260. doi:10.1371/journal.pone.0026260

    PubMed  Article  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

    PubMed  Article  CAS  Google Scholar 

  • Moldenhauer KAK, Lee FN, Gibbons JW, Bernhardt JL, Norman RJ, Slaton NA, Wilson CEK, Bulloch JM (2007) Registration of ‘Ahrent’ rice. Crop Sc 47:446–447

    Article  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    PubMed  Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Orgil U, Arakit H, Tangchaiburana S, Herkey R, Xiao S (2007) Intraspecific genetic variations fitness cost and benefit of rpw8 a disease resistance locus in Arabidopsis thaliana. Genetics 176:2317–2333

    PubMed  Article  CAS  Google Scholar 

  • Prim RC (1957) Shortest connection networks and some generalizations. Bell System Technical J 36:1389–1401

    Article  Google Scholar 

  • Rakshit S, Rakshit A, Matsumura H, Takahashi Y, Hasegawa Y, Ito A, Ishii T, Miyashita NT, Terauchi R (2007) Large scale DNA polymorphism study of Oryza sativa and Oryza rufipogon reveals the origin and divergence of Asian rice. Theor Appl Genet 114:731–743

    PubMed  Article  CAS  Google Scholar 

  • Rose IE, Bittner-eddy PD, Langley CH, Holub EB, Michelmore RW, Beyone JL (2004) The maintenance of extreme amino acid diversity at the disease resistance gene rpp13 in Arabidopsis thaliana. Genetics 166:1517–1527

    PubMed  Article  CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    PubMed  Article  CAS  Google Scholar 

  • Rybka K, Miyamoto M, Ando I, Saito A, Kawasaki S (1997) High resolution mapping of indica-derived rice blast resistance genes Pi-ta 2 and pi-ta and a consideration of their origin. Mol Plant Microbe-Interact 10:517–524

    Article  CAS  Google Scholar 

  • Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37(5):501–506

    PubMed  Article  CAS  Google Scholar 

  • Sharma TR, Rai AK, Gupta SK, Vijayan J, Devanna BN, Ray S (2012) Rice blast management through host-plant resistance: retrospect and prospects. Agri Res 1:37–52

    Article  Google Scholar 

  • Shen JH, Araki L, Chen JQ, Chen TD (2006) Unique evolutionary mechanism in R-genes under the presence/absence of polymorphism in Arabidopsis thaliana. Genetics 172:1243–1250

    PubMed  Article  CAS  Google Scholar 

  • Silue D, Notteghem JL, Tharreau D (1992) Evidence for a gene for gene relationship in the Oryza sativa-Magnaporthe grisea pathosystem. Phytopathology 82:577–582

    Article  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Thakur S, Singh PK, Rathour R, Variar M, Prashanthi SK, Singh AK, Singh UD, Chand D, Singh NK, Sharma TR (2012) Positive selection pressure on rice blast resistance allele Piz-t makes it divergent in Indian landraces. J Plant Interact. doi:10.1080/17429145.2012.721523

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive sequence alignment through sequence weighting, position-specific gaps penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680

    PubMed  Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    PubMed  Article  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

    PubMed  Article  CAS  Google Scholar 

  • Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Population Biol 7:256–276

    Article  CAS  Google Scholar 

  • Xia JQ, Correll JC, Lee FN, Rhoads DD, Marchetti MA (1993) DNA fingerprinting to examine variation in the Magnaporthe grisea (Pyricularia grisea) population in two rice fields in Arkansas. Phytopathology 83:1029–1035

    Article  CAS  Google Scholar 

  • Yang S, Gu T, Pan C, Feng Z, Ding J, Hang Y, Chen J, Tian D (2008) Genetic variation of NBS-LRR class resistance genes in rice lines. Theor Appl Genet 16:165–177

    Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

The financial assistance received from National Agricultural Innovation Project (NAIP) (C4/C1071), ICAR, by TR Sharma is gratefully acknowledged. The authors are thankful to the Officer in Charge, National Phytotron Facility, Indian Agricultural Research Institute, New Delhi, for providing basic facilities for growing and maintaining Indian local landraces. We also thank NCBI and various authors for making available sequence data of various Pi-ta alleles in the public domain.

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Authors and Affiliations

  1. National Research Centre on Plant Biotechnology, IARI, Pusa Campus, New Delhi, 110012, India

    S. Thakur, Y. K. Gupta, P. K. Singh, N. K. Singh & T. R. Sharma

  2. CSK Himachal Pradesh Agricultural University, Palampur, Himachal Pradesh, 176062, India

    R. Rathour

  3. Central Rainfed Upland Rice Research Station, CRRI, Hazaribagh, Jharkhand, 825301, India

    M. Variar

  4. University of Agricultural Sciences, Dharwad, Karnataka, 58001, India

    S. K. Prashanthi

  5. Indian Agricultural Research Institute, New Delhi, 110012, India

    A. K. Singh & U. D. Singh

  6. Himachal Pradesh University, Shimla, 171005, India

    S. Thakur & D. Chand

  7. NBPGR Regional Station, Shimla, 171003, India

    J. C. Rana

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  1. S. Thakur
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  2. Y. K. Gupta
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  3. P. K. Singh
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  4. R. Rathour
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  5. M. Variar
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  6. S. K. Prashanthi
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  7. A. K. Singh
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  8. U. D. Singh
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  9. D. Chand
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  10. J. C. Rana
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  11. N. K. Singh
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  12. T. R. Sharma
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Correspondence to T. R. Sharma.

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Thakur, S., Gupta, Y.K., Singh, P.K. et al. Molecular diversity in rice blast resistance gene Pi-ta makes it highly effective against dynamic population of Magnaporthe oryzae . Funct Integr Genomics 13, 309–322 (2013). https://doi.org/10.1007/s10142-013-0325-4

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  • DOI: https://doi.org/10.1007/s10142-013-0325-4

Keywords

  • Blast resistance gene
  • Haplotypes
  • Rice landraces
  • Magnaporthe oryzae
  • Oryza species
  • Pi-ta
  • Polymorphism