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Large-scale DNA polymorphism study of Oryza sativa and O. rufipogon reveals the origin and divergence of Asian rice

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Abstract

Polymorphism over ∼26 kb of DNA sequence spanning 22 loci and one region distributed on chromosomes 1, 2, 3 and 4 was studied in 30 accessions of cultivated rice, Oryza sativa, and its wild relatives. Phylogenetic analysis using all the DNA sequences suggested that O. sativa ssp. indica and ssp. japonica were independently domesticated from a wild species O. rufipogon. O. sativa ssp. indica contained substantial genetic diversity (π = 0.0024), whereas ssp. japonica exhibited extremely low nucleotide diversity (π = 0.0001) suggesting the origin of the latter from a small number of founders. O. sativa ssp. japonica contained a larger number of derived and fixed non-synonymous substitutions as compared to ssp. indica. Nucleotide diversity and genealogical history substantially varied across the 22 loci. A locus, RLD15 on chromosome 2, showed a distinct genealogy with ssp. japonica sequences distantly separated from those of O. rufipogon and O. sativa ssp. indica. Linkage disequilibrium (LD) was analyzed in two different regions. LD in O. rufipogon decays within 5 kb, whereas it extends to ∼50 kb in O. sativa ssp. indica.

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References

  • Akashi H (1995) Inferring weak selection from patterns of polymorphism and divergence at “silent” sites in Drosophila DNA. Genetics 139:1067–1076

    PubMed  CAS  Google Scholar 

  • Aquadro CF, Lado KM, Noon WA (1988) The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence. Genetics 119:875–888

    PubMed  CAS  Google Scholar 

  • Bautista NS, Solis R, Kamijima O, Ishii T (2001) RAPD, RFLP and SSLP analyses of phylogenetic relationships between cultivated and wild species of rice. Genes Genet Syst 77:71–79

    Article  Google Scholar 

  • Begun DJ, Aquadro CF (1992) Levels of naturally occurring DNA polymorphism correlate with recombination rates in Drosophila melanogaster. Nature 356:519–520

    Article  PubMed  CAS  Google Scholar 

  • Bennetzen JL (2000) Comparative sequence analysis of plant genomes: microcolinearity and its many exceptions. Plant Cell 12:1021–1029

    Article  PubMed  CAS  Google Scholar 

  • Chang TT (1995) Rice. In: Smartt J, Simmonds NW (eds) Evolution of crop plants. Longman, UK, pp 147–155

    Google Scholar 

  • Cheng C, Motohashi R, Tsuchimoto S, Fukuta Y, Ohtsubo H, Ohtshubo E (2003) Polyphyletic origin of cultivated rice: based on the interspersion pattern of SINEs. Mol Biol Evol 20:67–75

    Article  PubMed  CAS  Google Scholar 

  • Colbert T, Till BJ, Tompa R, Rynold S, Steine MN, Yeung AT, McCallum CM, Comai L, Henikoff S (2001) High-throughput screening for induced point mutations. Plant Physiol 126:480–484

    Article  PubMed  CAS  Google Scholar 

  • Comai L, Young K, Till BJ, Reynolds SH, Greene EA, Codomo CA, Enns LC, Johnson JE, Burtner C, Odden AR, Henikoff S (2004) Efficient discovery of DNA polymorphisms in natural populations by EcoTILLING. Plant J 37:778–786

    Article  PubMed  CAS  Google Scholar 

  • Eck RV, Dayhoff MO (1966) In: Dayhoff MO (ed) Atlas of protein sequence and structure. National Biomedical Research Foundation, Silver Springs

  • Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

    Google Scholar 

  • Felsenstein J, Churchill GA (1996) A Hidden Markov Model approach to variation among sites in rate of evolution. Mol Biol Evol 13:93–104

    PubMed  CAS  Google Scholar 

  • Feltus FA, Wan J, Shulze SR, Estill JC, Jiang N, Paterson AH (2004) An SNP resource for rice genetics and breeding based on subspecies indica and japonica genome alignments. Genome Res 14:1812–1819

    Article  PubMed  CAS  Google Scholar 

  • Ge S, Sang T, Lu BR, Hong DY (1999) Phylogeny of rice genomes with emphasis on origins of allotetraploid species. Proc Natl Acad Sci USA 96:14400–14405

    Article  PubMed  CAS  Google Scholar 

  • Gillespie JH (2004) Population genetics. A concise guide, 2nd edn. The Johns Hopkins University Press, Baltimore, pp 214

    Google Scholar 

  • Glinka S, Ometto L, Mousset S, Stephan W, De Lorenzo D (2003) Demography and natural selection have shaped genetic variation in Drosophila melanogaster: a multi-locus approach. Genetics 165:1269–1278

    PubMed  Google Scholar 

  • Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa ssp. japonica). Science 286:91–100

    Google Scholar 

  • Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57:461–485

    Article  PubMed  CAS  Google Scholar 

  • Harushima Y, Yano M, Shomura A, Sato M, Shimano T, Kuboki Y, Yamamoto T, Lin SY, Antonio BA, Parco A, Kajiya H, Huang N, Yamamoto K, Nagamura Y, Kurata N, Khush GS, Sasaki T (1998) A high-density rice genetic linkage map with 2275 markers using a single F2 population. Genetics 148:479–494

    PubMed  CAS  Google Scholar 

  • Hey J, Kliman RM (1993) Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Mol Biol Evol 10:804–822

    PubMed  CAS  Google Scholar 

  • Hill WG, Robertson A (1968) Linkage disequilibrium in finite populations. Theor Appl Genet 38:226–231

    Article  Google Scholar 

  • Hill WG, Weir BS (1988) Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol 33:54–78

    Article  PubMed  CAS  Google Scholar 

  • Hudson RR, Kaplan NL (1988) The coalescent process in models with selection and recombination. Genetics 111:147–164

    Google Scholar 

  • Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 136:1329–1340

    Google Scholar 

  • Ingvarsson PK (2005) Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European Aspen (Populus tremula L., Salicaceae). Genetics 169:945–953

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Ioerger TR, Clark AG, Kao TH (1991) Polymorphism at the self-incompatibility locus in Solanaceae predates speciation. Proc Natl Acad Sci USA 87:9732–9735

    Article  Google Scholar 

  • Ishii T, Terauchi T, Tsunewaki K (1988) Restriction endonuclease analysis of chloroplast DNA from A-genome diploid species of rice. Jpn J Genet 63:523–536

    Google Scholar 

  • Kawabe A, Miyashita NT (2003) Patterns of codon usage bias in three dicot and four monocot plant species. Genes Genet Syst 78:343–352

    Article  PubMed  CAS  Google Scholar 

  • Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34

    Article  PubMed  CAS  Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, London

    Google Scholar 

  • Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol 29:170–179

    Article  PubMed  CAS  Google Scholar 

  • Kliman RM, Andolfatto P, Coyne JA, Depaulis F, Kreitman M, Berry AJ, McCarter J, Wakely J, Hey J (2000) The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156:1913–1931

    PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lawlor DA, Ward FE, Ennis PD, Jackson AP, Parham P (1988) HLA-A and B polymorphisms predate the divergence of humans and chimpanzees. Nature 335:268–271

    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 

  • McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654

    Article  PubMed  CAS  Google Scholar 

  • Nasu S, Suzuki J, Ohta R, Hasegawa K, Yui R, Kitazawa N, Monna L, Minobe Y (2002) Search for and analysis of single nucleotide polymorphisms (SNPs) in rice (Oryza sativa, Oryza rufipogon) and establishment of SNP markers. DNA Res 9:163–171

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Nordborg M, Borevitz JO, Bergelson J, Berry CC, Chory J, Hagenblad J, Kreitman M, Maloof JN, Noyes T, Oefner PJ, Stahl EA, Weigel D (2002) The extent of linkage disequilibrium in Arabisopsis thaliana. Nat Genet 30:190–193

    Article  PubMed  CAS  Google Scholar 

  • Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, Zheng H, Bakker E, Calabrese P, Gladstone J, Goyal R, Jakobsson M, Kim S, Morozov Y, Padhukasahasram B, Plagnol V, Rosenberg NA, Shah C, Wall JD, Wang J, Zhao K, Kalbfleisch T, Schulz V, Kreitman M, Bergelson J (2005) The pattern of polymorphism in Arabidopsis thaliana. PLOS Biol 3:1289–1299

    Article  CAS  Google Scholar 

  • Ohta T (1976) Role of very slightly deleterious mutations in molecular evolution and polymorphism. Theor Popul Biol 10:254–275

    Article  PubMed  CAS  Google Scholar 

  • Oka HI (1988) Origin of cultivated rice. Japan Scientific Societies Press, Tokyo/Elsevier, Amsterdam

    Google Scholar 

  • Oka HI, Chang WT (1959) The impact of cultivation on populations of wild rice, Oryza sativa f. spontanea. Phyton 13:105–117

    Google Scholar 

  • Orengo DJ, Aguade M (2004) Detecting the footprint of positive selection in a European population of Drosophila melanogaster: multilocus pattern of variation and distance to coding regions. Genetics 167:1759–1766

    Article  PubMed  CAS  Google Scholar 

  • Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES 4th (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479–11484

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Second G (1982) Origin of the genic diversity of cultivated rice (Oryza spp.): study of the polymorphism scored at 40 isozyme loci. Jpn J Genet 57:25–57

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tajima F (1993) Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135:599–607

    PubMed  CAS  Google Scholar 

  • Vaughan DA, Morishima H, Kadowaki K (2003) Diversity in the Oryza genus. Curr Opin Plant Biol 6:139–146

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yoshida R, Miyashita NT, Ishii T (2004) Nucleotide polymorphism in the Adh1 locus region of the wild rice Oryza rufipogon. Theor Appl Genet 109:1406–1416

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M, Liu J, Sun J, Tang J, Chen Y, Huang X, Lin W, Ye C, Tong W, Cong L, Geng J, Han Y, Li L, Li W, Hu G, Huang X, Li W, Li J, Liu Z, Li L, Liu J, Qi Q, Liu J, Li L, Li T, Wang X, Lu H, Wu T, Zhu M, Ni P, Han H, Dong W, Ren X, Feng X, Cui P, Li X, Wang H, Xu X, Zhai W, Xu Z, Zhang J, He S, Zhang J, Xu J, Zhang K, Zheng X, Dong J, Zeng W, Tao L, Ye J, Tan J, Ren X, Chen X, He J, Liu D, Tian W, Tian C, Xia H, Bao Q, Li G, Gao H, Cao T, Wang J, Zhao W, Li P, Chen W, Wang X, Zhang Y, Hu J, Wang J, Liu S, Yang J, Zhang G, Xiong Y, Li Z, Mao L, Zhou C, Zhu Z, Chen R, Hao B, Zheng W, Chen S, Guo W, Li G, Liu S, Tao M, Wang J, Zhu L, Yuan L, Yang H (2002) A draft sequence of the rice genome (Oryza sativa L .ssp. indica). Science 296:79–92

    Article  PubMed  CAS  Google Scholar 

  • Zhu Q, Ge S (2005) Phylogenetic relationships among A-genome species of the genus Oryza revealed by intron sequences of four nuclear genes. New Phytol 167:249–265

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

SR conducted this work under financial support from Japanese Society for Promotion of Sciences, Tokyo. RT thanks B. Till, L. Comai and S. Henikoff, Washington University, Seatle, USA for training him with TILLING technique. We thank N. Kurata, National Institute of Genetics, Mishima, Japan for providing rice seeds, and J. Rozas, University of Barcelona, Spain for guiding us with the DnaSP program, two anonymous reviewers and M. Morgante, University of Udine, Italy for valuable comments to the earlier version of the manuscript. This work was supported by the “Program for Promotion of Basic Research Activities for Innovative Biosciences” (Japan), “Iwate University 21st Century COE Program: Establishment of Thermo-Biosystem Research Program” and “JSPS grant no. 18310136” to RT.

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Authors and Affiliations

  1. Iwate Biotechnology Research Center, Narita 22-174-4, Kitakami, 024-0003, Iwate, Japan

    Sujay Rakshit, Arunita Rakshit, Hideo Matsumura, Yoshihiro Takahashi, Yoshitaka Hasegawa, Akiko Ito & Ryohei Terauchi

  2. Indian Agricultural Research Institute, Pusa, New Delhi, 110012, India

    Sujay Rakshit

  3. Laboratory of Plant Breeding, Faculty of Agriculture, Kobe University, Kobe, 657-8501, Japan

    Takashige Ishii

  4. Laboratory of Plant Genetics, Graduate School of Agriculture, Kyoto University, Kyoto, 606-8502, Japan

    Naohiko T. Miyashita

  5. The United Graduate School of Agricultural Sciences, Iwate University, 3-18-8 Ueda, Morioka, Iwate, 020-8550, Japan

    Ryohei Terauchi

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  1. Sujay Rakshit
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Fig7

Supplementary Fig. 1. Results of multilocus HKA test. Contributions to the overall χ2 test static by the polymorphism and divergence observations for each locus. Squares indicate divergence between African and Asian species, and circles correspond to polymorphism within Asian species. If the observed value was greater than the expected, then the point is placed above the line; otherwise it is placed below the line (JPG 74 kb)

Supplementary Table 1. Plant materials used in the LD study (DOC 51 kb)

Supplementary Table 2. Summary of 22 loci studied (DOC 25 kb)

122_2006_473_MOESM3_ESM.doc

Supplementary Table 3. DNA polymorphism of O. sativa and O. rufipogon for silent positions (non-coding and coding synonymous sites) at the 22 loci (DOC 34 kb)

Supplementary Table 4. Contrasting levels of synonymous and replacement variation (DOC 33 kb)

122_2006_473_MOESM5_ESM.doc

Supplementary Table 5. Number of segregating sites within all positions (coding and non-coding positions) for Asian Oryza species (DOC 25 kb)

122_2006_473_MOESM6_ESM.doc

Supplementary Table 6. DNA variation in RLD15 locus (Only non-singleton mutations are shown. There were 67 singleton mutations specific to O. australiensis) (DOC 30 kb)

122_2006_473_MOESM7_ESM.doc

Supplementary Table 7. Shared polymorphism and fixed differences among O. sativa ssp. indica, ssp. japonica and O. rufipogon (DOC 33 kb)

Supplementary Table 8a. LD in O. rufipogon (XLS 23 kb)

Supplementary Table 8b. LD in O. sativa (XLS 23 kb)

Supplementary Table 8c. LD in O. sativa ssp. indica (XLS 24 kb)

Supplementary Table 8d. LD in O. sativa ssp. japonica (XLS 26 kb)

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Rakshit, S., Rakshit, A., Matsumura, H. et al. Large-scale DNA polymorphism study of Oryza sativa and O. rufipogon reveals the origin and divergence of Asian rice. Theor Appl Genet 114, 731–743 (2007). https://doi.org/10.1007/s00122-006-0473-1

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