Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Multiple domestications of Asian rice

Nature Plants volume 9, pages 1221–1235 (2023)Cite this article

Subjects

Abstract

The origin of domesticated Asian rice (Oryza sativa L.) has been controversial for more than half a century. The debates have focused on two leading hypotheses: a single domestication event in China or multiple domestication events in geographically separate areas. These two hypotheses differ in their predicted history of genes/alleles selected during domestication. Here we amassed a dataset of 1,578 resequenced genomes, including an expanded sample of wild rice from throughout its geographic range. We identified 993 selected genes that generated phylogenetic trees on which japonica and indica formed a monophyletic group, suggesting that the domestication alleles of these genes originated only once in either japonica or indica. Importantly, the domestication alleles of most selected genes (~80%) stemmed from wild rice in China, but the domestication alleles of a substantial minority of selected genes (~20%) originated from wild rice in South and Southeast Asia, demonstrating separate domestication events of Asian rice.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Population genetic structure and phylogenetic relationships of the wild and domesticated rice.
Fig. 2: Genetic variation patterns and population dynamics of wild and cultivated rice and domestication timeframes of cultivar groups.
Fig. 3: Whole-genome scans of PSRs and SORs in domesticated rice and phylogenetic analyses of domestication genes within the sweeps.
Fig. 4: Inference of origins of domestication alleles based on haplotype network analyses.
Fig. 5: Hypothesized domestication centres of Asian rice.

Similar content being viewed by others

Data availability

All newly resequenced genomes have been deposited in the National Center for Biotechnology Information Sequence Read Archive under number PRJNA705309. The genomic SNP data from all samples are available on Dryad (https://datadryad.org/stash/share/jcQfZcbai80MmLb6kO4_mrQLfu1tX-I_1_Yx7hAfJkI)91.

Code availability

All code and scripts used in the analyses are available at https://github.com/zhangfumin/domestication.

References

  1. Doebley, J. F., Gaut, B. S. & Smith, B. D. The molecular genetics of crop domestication. Cell 127, 1309–1321 (2006).

    Article  CAS  PubMed  Google Scholar 

  2. Allaby, R. G., Fuller, D. Q. & Brown, T. A. The genetic expectations of a protracted model for the origins of domesticated crops. Proc. Natl Acad. Sci. USA 105, 13982–13986 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Glemin, S. & Bataillon, T. A comparative view of the evolution of grasses under domestication. N. Phytol. 183, 273–290 (2009).

    Article  CAS  Google Scholar 

  4. Meyer, R. S. & Purugganan, M. D. Evolution of crop species: genetics of domestication and diversification. Nat. Rev. Genet. 14, 840–852 (2013).

    Article  CAS  PubMed  Google Scholar 

  5. Larson, G. et al. Current perspectives and the future of domestication studies. Proc. Natl Acad. Sci. USA 111, 6139–6146 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Gaut, B. S., Seymour, D. K., Liu, Q. & Zhou, Y. Demography and its effects on genomic variation in crop domestication. Nat. Plants 4, 512–520 (2018).

    Article  PubMed  Google Scholar 

  7. Chang, T.-T. The origin, evolution, cultivation, dissemination, and diversification of Asian and African rices. Euphytica 25, 425–441 (1976).

    Article  Google Scholar 

  8. Oka, H. Origin of Cultivated Rice (Elsevier, 1988).

  9. Gross, B. L. & Zhao, Z. Archaeological and genetic insights into the origins of domesticated rice. Proc. Natl Acad. Sci. USA 111, 6190–6197 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Khush, G. S. Origin, dispersal, cultivation and variation of rice. Plant Mol. Biol. 35, 25–34 (1997).

    Article  CAS  PubMed  Google Scholar 

  11. Fuller, D. Q. Contrasting patterns in crop domestication and domestication rates: recent archaeobotanical insights from the Old World. Ann. Bot. 100, 903–924 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Olsen, K. M. & Wendel, J. F. A bountiful harvest: genomic insights into crop domestication phenotypes. Annu. Rev. Plant Biol. 64, 47–70 (2013).

    Article  CAS  PubMed  Google Scholar 

  13. Sang, T. & Ge, S. Understanding rice domestication and implications for cultivar improvement. Curr. Opin. Plant Biol. 16, 139–146 (2013).

    Article  PubMed  Google Scholar 

  14. Kovach, M. J., Sweeney, M. T. & McCouch, S. R. New insights into the history of rice domestication. Trends Genet. 23, 578–587 (2007).

    Article  CAS  PubMed  Google Scholar 

  15. Sang, T. & Ge, S. Genetics and phylogenetics of rice domestication. Curr. Opin. Genet. Dev. 17, 533–538 (2007).

    Article  CAS  PubMed  Google Scholar 

  16. Wang, W. et al. Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature 557, 43–49 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. 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).

    Article  Google Scholar 

  18. Civan, P., Craig, H., Cox, C. J. & Brown, T. A. Three geographically separate domestications of Asian rice. Nat. Plants 1, 15164 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Vitte, C., Ishii, T., Lamy, F., Brar, D. & Panaud, O. Genomic paleontology provides evidence for two distinct origins of Asian rice (Oryza sativa L.). Mol. Genet. Genomics 272, 504–511 (2004).

    Article  CAS  PubMed  Google Scholar 

  20. 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).

    Article  CAS  PubMed  Google Scholar 

  21. He, Z. et al. Two evolutionary histories in the genome of rice: the roles of domestication genes. PLoS Genet. 7, e1002100 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Xu, X. et al. Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat. Biotechnol. 30, 105–111 (2012).

    Article  CAS  Google Scholar 

  23. Ishikawa, R., Castillo, C. C. & Fuller, D. Q. Genetic evaluation of domestication-related traits in rice: implications for the archaeobotany of rice origins. Archaeol. Anthropol. Sci. 12, 197 (2020).

    Article  Google Scholar 

  24. Vaughan, D. A., Lu, B.-R. & Tomooka, N. The evolving story of rice evolution. Plant Sci. 174, 394–408 (2008).

    Article  CAS  Google Scholar 

  25. Liu, R., Zheng, X.-M., Zhou, L., Zhou, H.-F. & Ge, S. Population genetic structure of Oryza rufipogon and Oryza nivara: implications for the origin of O. nivara. Mol. Ecol. 24, 5211–5228 (2015).

    Article  PubMed  Google Scholar 

  26. Cai, Z. et al. Parallel speciation of wild rice associated with habitat shifts. Mol. Biol. Evol. 36, 875–889 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Huang, X. et al. A map of rice genome variation reveals the origin of cultivated rice. Nature 490, 497–501 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Molina, J. et al. Molecular evidence for a single evolutionary origin of domesticated rice. Proc. Natl Acad. Sci. USA 108, 8351–8356 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Wang, H., Vieira, F. G., Crawford, J. E., Chu, C. & Nielsen, R. Asian wild rice is a hybrid swarm with extensive gene flow and feralization from domesticated rice. Genome Res. 27, 1029–1038 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Choi, J. Y. & Purugganan, M. D. Multiple origin but single domestication led to Oryza sativa. G3 (Bethesda) 8, 797–803 (2018).

    Article  CAS  PubMed  Google Scholar 

  32. Zhao, Q. et al. Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat. Genet. 50, 278–284 (2018).

    Article  CAS  PubMed  Google Scholar 

  33. Fuller, D. Q. Pathways to Asian civilizations: tracing the origins and spread of rice and rice cultures. Rice 4, 78–92 (2011).

    Article  Google Scholar 

  34. Bates, J., Petrie, C. A. & Singh, R. N. Approaching rice domestication in South Asia: new evidence from Indus settlements in northern India. J. Archaeol. Sci. 78, 193–201 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Glaszmann, J. C. Isozymes and classification of Asian rice varieties. Theor. Appl. Genet. 74, 21–30 (1987).

    Article  CAS  PubMed  Google Scholar 

  36. Wang, C. H. et al. Genetic diversity and classification of Oryza sativa with emphasis on Chinese rice germplasm. Heredity 112, 489–496 (2014).

    Article  CAS  PubMed  Google Scholar 

  37. Choi, J. Y. et al. The rice paradox: multiple origins but single domestication in Asian rice. Mol. Biol. Evol. 34, 969–979 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Yang, C.-C. et al. Independent domestication of Asian rice followed by gene flow from japonica to indica. Mol. Biol. Evol. 29, 1471–1479 (2012).

    Article  CAS  PubMed  Google Scholar 

  39. DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491–498 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

  41. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences. Nature 475, 493–496 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Liu, X. & Fu, Y.-X. Stairway Plot 2: demographic history inference with folded SNP frequency spectra. Genome Biol. 21, 280 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Terhorst, J., Kamm, J. A. & Song, Y. S. Robust and scalable inference of population history from hundreds of unphased whole genomes. Nat. Genet. 49, 303–309 (2017).

    Article  CAS  PubMed  Google Scholar 

  45. Zheng, X.-M. & Ge, S. Ecological divergence in the presence of gene flow in two closely related Oryza species (Oryza rufipogon and O. nivara). Mol. Ecol. 19, 2439–2454 (2010).

    Article  PubMed  Google Scholar 

  46. Cubry, P. et al. The rise and fall of African rice cultivation revealed by analysis of 246 new genomes. Curr. Biol. 28, 2274–2282 (2018).

    Article  CAS  PubMed  Google Scholar 

  47. Schmutz, J. et al. A reference genome for common bean and genome-wide analysis of dual domestications. Nat. Genet. 46, 707–713 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Zhao, G. et al. A comprehensive genome variation map of melon identifies multiple domestication events and loci influencing agronomic traits. Nat. Genet. 51, 1607–1615 (2019).

    Article  CAS  PubMed  Google Scholar 

  49. Zhang, K. et al. Resequencing of global Tartary buckwheat accessions reveals multiple domestication events and key loci associated with agronomic traits. Genome Biol. 22, 23 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Nielsen, R. et al. Genomic scans for selective sweeps using SNP data. Genome Res. 15, 1566–1575 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  52. Gutaker, R. M. et al. Genomic history and ecology of the geographic spread of rice. Nat. Plants 6, 492–502 (2020).

    Article  PubMed  Google Scholar 

  53. Civan, P. et al. Origin of the Aromatic group of cultivated rice (Oryza sativa L.) traced to the Indian subcontinent. Genome Biol. Evol. 11, 832–843 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Choi, J. Y. et al. Nanopore sequencing-based genome assembly and evolutionary genomics of circum-basmati rice. Genome Biol. 21, 21 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Nosil, P. Ecological Speciation (Oxford Univ. Press, 2012).

  56. Via, S. Natural selection in action during speciation. Proc. Natl Acad. Sci. USA 106, 9939–9946 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Ronco, F. et al. Drivers and dynamics of a massive adaptive radiation in cichlid fishes. Nature 589, 76–81 (2021).

    Article  CAS  PubMed  Google Scholar 

  61. Schiffels, S. & Durbin, R. Inferring human population size and separation history from multiple genome sequences. Nat. Genet. 46, 919–925 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Schiffels, S. & Wang, K. in Statistical Population Genomics (ed. Dutheilm, J. Y.) 147–166 (Springer US, 2020).

  63. Thomas, C. G. et al. Full-genome evolutionary histories of selfing, splitting, and selection in Caenorhabditis. Genome Res. 25, 667–678 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Meyer, R. S. et al. Domestication history and geographical adaptation inferred from a SNP map of African rice. Nat. Genet. 48, 1083–1088 (2016).

    Article  CAS  PubMed  Google Scholar 

  65. Hudson, R. R., Slatkin, M. & Maddison, W. P. Estimation of levels of gene flow from DNA sequence data. Genetics 132, 583–589 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Weigand, H. & Leese, F. Detecting signatures of positive selection in non-model species using genomic data. Zool. J. Linn. Soc. 184, 528–583 (2018).

    Article  Google Scholar 

  67. Sakai, H. et al. Rice Annotation Project Database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol. 54, e6 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Felsenstein, J. PHYLIP—phylogeny inference package (version 3.2). Cladistics 5, 164–166 (1989).

    Google Scholar 

  69. Banaticla-Hilario, M. C. N., McNally, K. L., van den Berg, R. G. & Sackville Hamilton, N. R. Crossability patterns within and among Oryza series Sativae species from Asia and Australia. Genet. Resour. Crop Evol. 60, 1899–1914 (2013).

    Article  Google Scholar 

  70. Tajima, F. Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460 (1983).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Watterson, G. A. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7, 256–276 (1975).

    Article  CAS  PubMed  Google Scholar 

  72. Zhang, C., Dong, S.-S., Xu, J.-Y., He, W.-M. & Yang, T.-L. PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics 35, 1786–1788 (2019).

    Article  CAS  PubMed  Google Scholar 

  73. Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. R Core Team. R: A Language and Environment for Statistical Computing version 3.2.1 (R Foundation for Statistical Computing, 2015).

  76. Yang, J., Lee, S. H., Goddard, M. E. & Visscher, P. M. GCTA: a tool for genome-wide complex trait analysis. Am. J. Hum. Genet. 88, 76–82 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).

  78. Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Bouckaert, R. R. DensiTree: making sense of sets of phylogenetic trees. Bioinformatics 26, 1372–1373 (2010).

    Article  CAS  PubMed  Google Scholar 

  80. Yamamoto, E., Yonemaru, J.-i, Yamamoto, T. & Yano, M. OGRO: the overview of functionally characterized genes in rice online database. Rice 5, 26 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  81. Yao, W., Li, G., Yu, Y. & Ouyang, Y. funRiceGenes dataset for comprehensive understanding and application of rice functional genes. GigaScience 7, 1–9 (2018).

    Article  PubMed  Google Scholar 

  82. Todesco, M. et al. Massive haplotypes underlie ecotypic differentiation in sunflowers. Nature 584, 602–607 (2020).

    Article  CAS  PubMed  Google Scholar 

  83. Browning, B. L., Zhou, Y. & Browning, S. R. A one-penny imputed genome from next-generation reference panels. Am. J. Hum. Genet. 103, 338–348 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Bandelt, H.-J., Forster, P. & Rohl, A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48 (1999).

    Article  CAS  PubMed  Google Scholar 

  85. Bowman, A. W. & Azzalini, A. sm: Smoothing methods for nonparametric regression and density estimation. R package version 2.2-5.7 http://www.stats.gla.ac.uk/~adrian/sm (2021).

  86. Pebesma, E. Simple features for R: standardized support for spatial vector data. R J. 10, 439–446 (2018).

    Article  Google Scholar 

  87. Green, R. E. et al. A draft sequence of the neandertal genome. Science 328, 710–722 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Durand, E. Y., Patterson, N., Reich, D. & Slatkin, M. Testing for ancient admixture between closely related populations. Mol. Biol. Evol. 28, 2239–2252 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Stein, J. C. et al. Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza. Nat. Genet. 50, 285–296 (2018).

    Article  CAS  PubMed  Google Scholar 

  90. Ma, X. et al. Whole-genome de novo assemblies reveal extensive structural variations and dynamic organelle-to-nucleus DNA transfers in African and Asian rice. Plant J. 104, 596–612 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Zhang, F.-M., Jing, C.-Y. & Ge, S. Genomic SNP data for domestication research of Asian cultivated rice. Dryad https://doi.org/10.5061/dryad.xksn02vjd (2022).

Download references

Acknowledgements

We thank T. Sang, Y.-L. Guo and J.-L. Li for discussion and suggestions; B.-R. Lu, W.-L. Chen and D. Ratnasekera for field collections; X.-H. Wei, C.-B. Chen, H.-Z. Zeng and other members of S.G.’s laboratory for phenotyping and lab assistance; and A.-L. Li for picture drawing. We also thank the International Rice Research Institute (Los Banos, Philippines) and the China National Rice Research Institute (CNRRI) (Hangzhou, China) for providing seed samples and the CNRRI, the Guangxi Academy of Agricultural Sciences (Nanning, China) and the CAS Field Station (Lingshui, China) for providing the experimental fields. This work was financially supported by funding from the National Natural Science Foundation of China (grant no. 91231201), the Strategic Priority Research Program of Chinese Academy of Sciences (grant nos. XDB31000000 and XDA08020103) and the Ministry of Science and Technology (grant no. 2021YFD1200101-02) to S.G.; the National Natural Science Foundation of China (grant nos. 91731301 and 32130008 to S.G., 31470332 to F.-M.Z. and 31800186 to Z.C.); and the China Postdoctoral Science Foundation (grant no. 2017M620950 to Z.C.).

Author information

Author notes

  1. These authors contributed equally: Chun-Yan Jing, Fu-Min Zhang, Xiu-Hua Wang, Mei-Xia Wang.

Authors and Affiliations

  1. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China

    Chun-Yan Jing, Fu-Min Zhang, Xiu-Hua Wang, Mei-Xia Wang, Lian Zhou, Zhe Cai, Jing-Dan Han, Mu-Fan Geng, Wen-Hao Yu, Zi-Hui Jiao, Lei Huang, Rong Liu, Xiao-Ming Zheng, Qing-Lin Meng, Ning-Ning Ren, Hong-Xiang Zhang, Yu-Su Du, Xin Wang, Cheng-Gen Qiang, Xin-Hui Zou & Song Ge

  2. University of Chinese Academy of Sciences, Beijing, China

    Chun-Yan Jing, Fu-Min Zhang, Xiu-Hua Wang, Mei-Xia Wang, Mu-Fan Geng, Wen-Hao Yu, Zi-Hui Jiao, Qing-Lin Meng, Ning-Ning Ren, Hong-Xiang Zhang, Yu-Su Du, Xin Wang, Cheng-Gen Qiang, Xin-Hui Zou & Song Ge

  3. Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China

    Rong Liu & Xiao-Ming Zheng

  4. University of California, Irvine, Irvine, CA, USA

    Brandon S. Gaut

Authors
  1. Chun-Yan Jing
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fu-Min Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiu-Hua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mei-Xia Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lian Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhe Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jing-Dan Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mu-Fan Geng
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Wen-Hao Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zi-Hui Jiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Lei Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Rong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Xiao-Ming Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Qing-Lin Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Ning-Ning Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Hong-Xiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Yu-Su Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Xin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Cheng-Gen Qiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Xin-Hui Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Brandon S. Gaut
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Song Ge
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S.G. conceived and designed the project. S.G. and F.-M.Z. supervised the research. C.-Y.J., X.-H.W., F.-M.Z., M.-X.W., L.Z. and L.H. obtained and analysed the genomic data. F.-M.Z., S.G., C.-Y.J., Z.C., X.-H.W., M.-X.W. and L.Z. performed the population genetic analyses. F.-M.Z., M.-X.W., W.-H.Y. and C.-Y.J. performed the haplotype analyses. S.G., L.Z., M.-X.W., M.-F.G., Q.-L.M., N.-N.R., X.-M.Z., R.L., L.H., Y.-S.D., X.W. and C.-G.Q. conducted the field collections and phenotyping. L.Z., M.-F.G., Q.-L.M., J.-D.H., Z.-H.J., H.-X.Z. and X.-H.Z. were involved in lab assistance. S.G., B.S.G. and F.-M.Z. wrote the manuscript with help from all co-authors.

Corresponding author

Correspondence to Song Ge.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Plants thanks Feng Tian, Paul Gepts and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Morphology and diagnostic features of wild rice (O. rufipogon and O. nivara) and domesticated rice (O. sativa).

a, b, c. Panicles of O. rufipogon, O. nivara and Nipponbare (O. sativa ssp. japonica) in heading stage, respectively, which were indicated by red boxes in the bottom panel. d. Gross morphology of O. rufipogon (accession no. NEP04X4), O. nivara (accession no. NEP0202a) and Nipponbare. Two wild species were sampled from Nepal and were grown in the common garden in Beijing, together with Nipponbare. e. A list of diagnostic features to delineate wild rice and domesticated rice.

Extended Data Fig. 2 Analyses of population genetic structure of two wild rice species (O. rufipgon and O. nivara).

a. Neighbor-joining tree of 457 wild rice accessions. Lines in colors represent two species. The scale bar shows substitutions per site. b. Principal components of 457 wild rice accessions with mislabeled and admixed accessions indicated. Dots in colors indicate four genetic lineages and those in grey indicate admixed accessions. c. ADMIXTURE plots for 404 wild rice accessions excluding admixed accessions. Four different lineages are indicated above the plots. The columns represent the accessions with their origins indicated below the plots.

Extended Data Fig. 3 Analyses of population genetic structure of Asian rice based on 1121 rice landraces with mislabeled and admixed accessions indicated.

a. Neighbor-joining tree of 1121 rice landraces. Lines in colors represent six cultivar groups originally defined. The scale bar shows substitutions per site. b. Principal components of 1121 rice landraces. Dots in colors indicate six cultivar groups and those in grey indicate admixed accessions. c. ADMIXTURE plots for rice landraces. Two rice subspecies are indicated above the plots. Columns represent the landraces with the cultivar groups indicated below the plots.

Extended Data Fig. 4 Genome-wide linkage disequilibrium (LD) of wild and domesticated rice.

a, b. Comparisons of LD patterns for two wild species (O. rufipogon and O. nivara) and two rice subspecies (Japonica and Indica). c, d. LD patterns of four lineages of wild species (c) and six cultivar groups (d). The x axis is the physical distance between pair of SNPs (kb) in wild and domesticated rice. The y axis is the squared allele-frequency correlations r2.

Extended Data Fig. 5 Phylogenetic relationships of major lineages of wild rice and major cultivar groups of rice landraces.

a. NJ tree of 1493 wild and domesticated rice accessions based on genetic distance calculated with neutral loci. b. NJ tree of 1355 wild and domesticated rice (japonica and indica) based on genetic distance calculated with neutral loci. c. NJ tree of 1355 wild and main cultivar groups based on all SNPs. Lines in colors represent wild lineages and cultivar groups. The scale bar shows substitutions per site. d, e. NJ trees constructed individually by 34,291 genes annotated based on all four wild lineages and six cultivar groups (d) and based on four wild lineages and three major cultivar groups (e). Heavy red lines indicate the cladogram supported by a majority of gene trees. Numbers near the nodes represent proportion of the genes that resolved notes on their trees. japonica = temperate japonica + tropical japonica.

Extended Data Fig. 6 Illustration of a new strategy to distinguish between single and multiple domestications based on phylogenetic analysis of single-origin selective sweep regions (SORs)/single-origin selected genes (SOGs).

a. Identification of the genomic region/gene under selection common to both japonica and indica, defined as a putative selective sweep region (PSR)/putative selected gene (PSG). b. Determination of the PSR/PSG of single origin, that is, the PSR/PSG that generated a tree on which japonica and indica formed a group (cultivar group), defined as a single-origin selective sweep region (SOR)/single-origin selected gene (SOG). c. Test for hypotheses based on the phylogenetic trees of SORs/SOGs. A single domestication model is supported if the same wild lineage is sister to a cultivar group on the trees (left) and a multiple domestication model is supported if multiple wild lineages cluster with cultivar groups on different trees (right). Three lines above the panel indicate the diversity of wild (blue), indica (orange) and japonica (green) samples, respectively. Wild-A and Wild-B represent different wild lineages.

Extended Data Fig. 7 Genome-wide scan of putative selective sweep regions (PSRs) and single-origin selective sweep regions (SORs) in domesticated rice across 12 chromosomes.

Nucleotide diversity (π) and its ratio (RODW/C) of wild to domesticated populations and divergence (FST) between wild and domesticated populations are plotted for 100kb sliding windows against the position across chromosomes. Dots in red are the outliers with RODW/C and FST values over the thresholds in japonica and indica. Black rectangles on the chromosomes represent the centromeres. The shaded regions on chromosomes 4 and 7 are SOR33 and SOR48, respectively.

Extended Data Fig. 8 Schematic diagram of two single-origin selective sweep regions (SORs) (SOR33 and SOR48) and NJ trees of domestication genes within the SORs.

a. SOR33 locates on chromosome 4 and includes LABA1 (with domestication alleles from indica) and LCBK2 (with domestication alleles from japonica) genes. b. SOR48 locates on chromosome 7 and includes PROG1 (with domestication alleles from japonica) and GLO4 (with domestication alleles from indica) genes. NJ trees were constructed using the SNPs extracted from three fragments spanning the gene, that is, the gene only, the gene and its 1 kb upstream and downstream regions (gene ± 1k), the gene and its 3 kb upstream and downstream 3 kb regions (gene ± 3k). Bootstrap supports over 60% are shown near the nodes.

Extended Data Table 1 Results of D-statistics (a) and three-population test (f3) (b) to quantify gene flow
Full size table

Supplementary information

Supplementary Information

Supplementary Figs. 1–19; Tables 1, 4–8, 14, 17, 21, 23 and 24; and text.

Reporting Summary

Supplementary Data

Supplementary Tables 2, 3, 9–13, 15, 16, 18–20, 22 and 25.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jing, CY., Zhang, FM., Wang, XH. et al. Multiple domestications of Asian rice. Nat. Plants 9, 1221–1235 (2023). https://doi.org/10.1038/s41477-023-01476-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-023-01476-z

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing