Rice is a staple crop that has undergone substantial phenotypic and physiological changes during domestication. Here we resequenced the genomes of 40 cultivated accessions selected from the major groups of rice and 10 accessions of their wild progenitors (Oryza rufipogon and Oryza nivara) to >15 × raw data coverage. We investigated genome-wide variation patterns in rice and obtained 6.5 million high-quality single nucleotide polymorphisms (SNPs) after excluding sites with missing data in any accession. Using these population SNP data, we identified thousands of genes with significantly lower diversity in cultivated but not wild rice, which represent candidate regions selected during domestication. Some of these variants are associated with important biological features, whereas others have yet to be functionally characterized. The molecular markers we have identified should be valuable for breeding and for identifying agronomically important genes in rice.
Subscribe to Journal
Get full journal access for 1 year
only $20.83 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Kovach, M.J., Sweeney, M.T. & McCouch, S.R. New insights into the history of rice domestication. Trends Genet. 23, 578–587 (2007).
Sang, T. & Ge, S. Genetics and phylogenetics of rice domestication. Curr. Opin. Genet. Dev. 17, 533–538 (2007).
Li, C., Zhou, A. & Sang, T. Rice domestication by reducing shattering. Science 311, 1936–1939 (2006).
Sweeney, M.T., Thomson, M.J., Pfeil, B.E. & McCouch, S. Caught red-handed: Rc encodes a basic helix-loop-helix protein conditioning red pericarp in rice. Plant Cell 18, 283–294 (2006).
Jin, J. et al. Genetic control of rice plant architecture under domestication. Nat. Genet. 40, 1365–1369 (2008).
Tan, L. et al. Control of a key transition from prostrate to erect growth in rice domestication. Nat. Genet. 40, 1360–1364 (2008).
Huang, X. et al. Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42, 961–967 (2010).
Hirschhorn, J.N. & Daly, M.J. Genome-wide association studies for common diseases and complex traits. Nat. Rev. Genet. 6, 95–108 (2005).
He, Z. et al. Two evolutionary histories in the genome of rice: the roles of domestication genes. PLoS Genet. 7, e1002100 (2011).
Glaszmann, J.C. Isozymes and classification of Asian rice varieties. Theor. Appl. Genet. 74, 21–30 (1987).
Garris, A.J., Tai, T.H., Coburn, J., Kresovich, S. & McCouch, S. Genetic structure and diversity in Oryza sativa L. Genetics 169, 1631–1638 (2005).
International Rice Genome Sequencing Project. The map-based sequence of the rice genome. Nature 436, 793–800 (2005).
Goff, S.A. et al. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296, 92–100 (2002).
Li, R. et al. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966–1967 (2009).
Zdobnov, E.M. & Apweiler, R. InterProScan—an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17, 847–848 (2001).
Korbel, J.O. et al. Paired-end mapping reveals extensive structural variation in the human genome. Science 318, 420–426 (2007).
Campbell, P.J. et al. Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing. Nat. Genet. 40, 722–729 (2008).
Tuzun, E. et al. Fine-scale structural variation of the human genome. Nat. Genet. 37, 727–732 (2005).
Charlesworth, D. & Willis, J.H. The genetics of inbreeding depression. Nat. Rev. Genet. 10, 783–796 (2009).
Fu, H. & Dooner, H.K. Intraspecific violation of genetic colinearity and its implications in maize. Proc. Natl. Acad. Sci. USA 99, 9573–9578 (2002).
Springer, N.M. & Stupar, R.M. Allelic variation and heterosis in maize: how do two halves make more than a whole? Genome Res. 17, 264–275 (2007).
McNally, K.L. et al. Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. Proc. Natl. Acad. Sci. USA 106, 12273–12278 (2009).
Clark, R.M. et al. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317, 338–342 (2007).
Lam, H.M. et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat. Genet. 42, 1053–1059 (2010).
Tanksley, S.D. & McCouch, S.R. Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277, 1063–1066 (1997).
Tajima, F. Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460 (1983).
Caicedo, A.L. et al. Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet. 3, e163 (2007).
Second, G. 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 (1982).
Zhu, Q. & Ge, S. Phylogenetic relationships among A-genome species of the genus Oryza revealed by intron sequences of four nuclear genes. New Phytol. 167, 249–265 (2005).
Londo, J.P., Chiang, Y.C., Hung, K.H., Chiang, T.Y. & Schaal, B.A. Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proc. Natl. Acad. Sci. USA 103, 9578–9583 (2006).
Menozzi, P., Piazza, A. & Cavalli-Sforza, L. Synthetic maps of human gene frequencies in Europeans. Science 201, 786–792 (1978).
Patterson, N., Price, A.L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006).
Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425 (1987).
Tamura, K., Dudley, J., Nei, M. & Kumar, S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599 (2007).
Tang, H., Peng, J., Wang, P. & Risch, N.J. Estimation of individual admixture: analytical and study design considerations. Genet. Epidemiol. 28, 289–301 (2005).
Li, R. et al. SNP detection for massively parallel whole-genome resequencing. Genome Res. 19, 1124–1132 (2009).
Fuller, D.Q. et al. The domestication process and domestication rate in rice: spikelet bases from the Lower Yangtze. Science 323, 1607–1610 (2009).
Hill, W.G. & Robertson, A. Linkage disequilibrium in finite populations. TAG Theoretical and Applied Genetics 38, 226–231 (1968).
Barrett, J.C., Fry, B., Maller, J. & Daly, M.J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263–265 (2005).
Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595 (1989).
Tenaillon, M.I., U'Ren, J., Tenaillon, O. & Gaut, B.S. Selection versus demography: a multilocus investigation of the domestication process in maize. Mol. Biol. Evol. 21, 1214–1225 (2004).
Wright, S.I. et al. The effects of artificial selection on the maize genome. Science 308, 1310–1314 (2005).
Yamasaki, M. et al. A large-scale screen for artificial selection in maize identifies candidate agronomic loci for domestication and crop improvement. Plant Cell 17, 2859–2872 (2005).
Yamasaki, M., Wright, S.I. & McMullen, M.D. Genomic screening for artificial selection during domestication and improvement in maize. Ann. Bot. 100, 967–973 (2007).
Gibbs, R.A. et al. Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds. Science 324, 528–532 (2009).
Xia, Q. et al. Complete resequencing of 40 genomes reveals domestication events and genes in silkworm (Bombyx). Science 326, 433–436 (2009).
Rubin, C.J. et al. Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 464, 587–591 (2010).
Wright, S. Evolution and the Genetics of Populations (The University of Chicago Press, Chicago, 1977).
Jain, M. & Khurana, J.P. Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J. 276, 3148–3162 (2009).
Paponov, I.A. et al. The evolution of nuclear auxin signalling. BMC Evol. Biol. 9, 126 (2009).
Retief, J.D. Phylogenetic analysis using PHYLIP. Methods Mol. Biol. 132, 243–258 (2000).
Zhu, Q., Zheng, X., Luo, J., Gaut, B.S. & Ge, S. Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Mol. Biol. Evol. 24, 875–888 (2007).
Wang, J. et al. The diploid genome sequence of an Asian individual. Nature 456, 60–65 (2008).
Li, R., Li, Y., Kristiansen, K. & Wang, J. SOAP: short oligonucleotide alignment program. Bioinformatics 24, 713–714 (2008).
Li, R. et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 20, 265–272 (2010).
Stanke, M., Schoffmann, O., Morgenstern, B. & Waack, S. Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources. BMC Bioinformatics 7, 62 (2006).
Yi, X. et al. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329, 75–78 (2010).
Li, Y. et al. Structural variation in two human genomes mapped at single-nucleotide resolution by whole genome de novo assembly. Nat. Biotech. 29, 723–730 (2011).
Kent, W.J. BLAT—The BLAST-Like Alignment Tool. Genome Res. 12, 656–664 (2002).
Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
Watterson, G.A. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7, 256–276 (1975).
Hudson, R.R., Slatkin, M. & Maddison, W.P. Estimation of levels of gene flow from DNA sequence data. Genetics 132, 583–589 (1992).
Tanaka, T. et al. The Rice Annotation Project Database (RAP-DB): 2008 update. Nucleic Acids Res. 36, D1028–D1033 (2008).
We thank C.-H. Shi (Zhejiang University, China) and X.-H. Wei (China National Rice Research Institute) for assistance in growing rice materials. We are grateful to the International Rice Research Institute (Los Banos, Philippines) for providing most seed samples. This work was supported by the Chinese 973 program (2007CB815700), the National Natural Science Foundation of China (30990242), the Provincial Key Grant of Yunnan Province (2008CC017; 2008GA002), the Shenzhen Municipal Government and the Yantian District local government of Shenzhen, the Ole Rømer grant from the Danish Natural Science Research Council, and a CAS-Max Planck Society Fellowship and the 100 talent program of CAS to W.W., J.W. and S.G. We also acknowledge funding support from the Chinese Ministry of Agriculture (948 program), the Shenzhen Municipal Government of China and grants from Shenzhen Bureau of Science Technology & Information, China (ZYC200903240077A; CXB200903110066A).
The authors declare no competing financial interests.
Supplementary Tables 1,2,5,6,8–16, Supplmentary Notes and Supplementary Figures 1–23 (PDF 4530 kb)
Annotation information of novel genes identified from unmapped contigs. (XLSM 156 kb)
Information of lost genes. (+ means not lost in that individual, - mean lost supported by both pairs and coverage information, P means only supported by pair-end information, C means only supported by coverage information.) (XLSM 202 kb)
CNV regions. (XLSM 72 kb)
About this article
Cite this article
Xu, X., Liu, X., Ge, S. et al. Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30, 105–111 (2012) doi:10.1038/nbt.2050
Molecular Plant (2019)
Comparative transcriptomics analysis uncovers alternative splicing events and molecular markers in cabbage (Brassica oleracea L.)
Genome Research (2019)
Detection of a novel locus involved in non-seed-shattering behaviour of Japonica rice cultivar, Oryzasativa ‘Nipponbare’
Theoretical and Applied Genetics (2019)
Epigenetic modification of ESP, encoding a putative long noncoding RNA, affects panicle architecture in rice