遺伝イネゲノムの変異マップから栽培イネの起源が判明

Journal name:
Nature
Volume:
490,
Pages:
497–501
Date published:
DOI:
doi:10.1038/nature11532
Received
Accepted
Published online

Abstract

作物の栽培化は長期にわたる選択の実験であり、これがヒトの文明を大きく進歩させてきた。栽培イネ( Oryza sativa L.)の栽培化は、歴史上最も重要な進歩の1つに位置付けられるが、その起源と栽培化の過程については意見が分かれており、長く論争が続いてきた。今回我々は、さまざまな地域から収集した野生イネ、ルフィポゴン( Oryza rufipogon 、栽培イネを生み出した直接の祖先種)の446系統と、栽培イネであるインディカイネとジャポニカイネの1,083系統について、ゲノム塩基配列を解読し、イネゲノムの包括的な変異マップを作成した。選択の痕跡を探索して、栽培化の過程で選択的除去(selective sweep)が起こった55の領域を同定した。この選択的除去とゲノム全域の変異パターンを綿密に解析したところ、ジャポニカイネ( Oryza sativa japonica )は初め、中国南部の珠江中流領域周辺でルフィポゴンの1集団から栽培化されたことが判明した。またインディカイネ( Oryza sativa indica )は、最初に生まれた栽培イネがその後、東南アジアや南アジアに広がるにつれ、このジャポニカイネと現地の野生イネとの交配により生じたことも明らかになった。高精度の遺伝子マップ作成により、栽培化に関係する形質の解析も行った。この研究は、イネの育種のための重要な基盤となり、また作物の栽培化の研究に役立つ効果的なゲノミクス手法を示している。

At a glance

Figures

  1. Genetic structure and association analysis in the wild rice population.
    Figure 1: Genetic structure and association analysis in the wild rice population.

    a, Neighbour-joining tree of 446 O. rufipogon accessions, which was calculated from ~5 million SNPs, identifies the three groups of Or-I (red), Or-II (grey) and Or-III (blue). b, Geographic origins of wild rice accessions. c, The level of genetic differentiation (FST) in O. rufipogon population around the DPL2 gene that underlies indicajaponica hybrid incompatibility in rice. d, Regional Manhattan plots of GWAS for tiller angle in O. rufipogon population identify a known gene, PROG1, using a compressed mixed linear model. The genome-wide significance threshold (1×10−6) and the position of the peak SNP are indicated by a horizontal dash-dot line and a vertical red line, respectively.

  2. Genome-wide relationship between cultivated rice and its wild progenitor.
    Figure 2: Genome-wide relationship between cultivated rice and its wild progenitor.

    a, Phylogenetic tree of the full population (446 O. rufipogon accessions and 1,083 O. sativa varieties) calculated from ~8 million SNPs in O. rufipogon and O. sativa. The double-layer rings indicate O. rufipogon (outer ring: Or-I, Or-II and Or-III are coloured in red, grey and blue, respectively) and O. sativa (inner ring: indica and japonica subspecies are in pink and sky blue, respectively). b, Illustration of genetic diversity and population differentiation in O. rufipogon and O. sativa. The size of the circles represents the level of genetic diversity (π) of the groups, and the FST values between the groups are indicated. ind, indica; jap, japonica. c, The spectrum of allele frequencies at the causal polymorphisms of Ghd7, DPL2 and GS3.

  3. Whole-genome screening and functional annotations of domestication sweeps.
    Figure 3: Whole-genome screening and functional annotations of domestication sweeps.

    a, Whole-genome screening of domestication sweeps in the full population of O. rufipogon and O. sativa. The values of πw/πc are plotted against the position on each chromosome. The horizontal dashed line indicates the genome-wide threshold of selection signals (πw/πc>3). bd, A large-scale high-resolution mapping for fifteen domestication-related traits was performed in an O. rufipogon×O. sativa population. The domestication sweeps overlapped with characterized domestication-related QTLs are shown in dark red, and the loci with known causal genes are shown in red. Among them, three strong selective sweeps were found to be associated with grain width (b), grain weight (c) and exserted stigma (d), respectively. In bd, the likelihood of odds (LOD) values from the composite interval mapping method are plotted against position on the rice chromosomes. Grey horizontal dashed line indicates the threshold (LOD>3.5).

  4. Genetic and geographic origins of rice domestication.
    Figure 4: Genetic and geographic origins of rice domestication.

    a, Phylogenetic tree of 446 O. rufipogon accessions and 1,083 O. sativa varieties calculated from SNPs in the overall regions of the 55 major domestication sweeps. b, Geographic locations of 62 O. rufipogon accessions, whose phylogenetic positions during domestication are indicated. Colour index represents the average of the genetic distance of O. rufipogon accessions to all cultivated rice accessions. Two major rivers in southern China are labelled in grey in the map. c, The average distance of O. rufipogon accessions from different countries to all cultivars. The distance was estimated by simple matching distance of SNPs around the Bh4 locus or all SNPs within the 55 domestication sweeps. d, The average distance of O. rufipogon accessions from different provinces in southern China to all cultivars. e, Schematics of the origin of cultivated rice. The aus and aromatic rice are minor groups of rice accessions with small geographic distributions.

Accession codes

Primary accessions

European Nucleotide Archive

References

  1. Oka, H. I. Origin of cultivated rice. (Japan Scientific Societies Press, 1988)
  2. Khush, G. S. Origin, dispersal, cultivation and variation of rice. Plant Mol. Biol. 35, 2534 (1997)
  3. Cheng, C. et al. Polyphyletic origin of cultivated rice: based on the interspersion pattern of SINEs. Mol. Biol. Evol. 20, 6775 (2003)
  4. Fuller, D. Q. et al. Consilience of genetics and archaeobotany in the entangled history of rice. Archaeol. Anthropol. Sci. 2, 115131 (2010)
  5. Li, C., Zhou, A. & Sang, T. Genetic analysis of rice domestication syndrome with the wild annual species, Oryza nivara. New Phytol. 170, 185194 (2006)
  6. Li, C., Zhou, A. & Sang, T. Rice domestication by reducing shattering. Science 311, 19361939 (2006)
  7. Jin, J. et al. Genetic control of rice plant architecture under domestication. Nature Genet. 40, 13651369 (2008)
  8. Tan, L. et al. Control of a key transition from prostrate to erect growth in rice domestication. Nature Genet. 40, 13601364 (2008)
  9. Zhu, B. F. et al. Genetic control of a transition from black to straw-white seed hull in rice domestication. Plant Physiol. 155, 13011311 (2011)
  10. 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, 95789583 (2006)
  11. Caicedo, A. L. et al. Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet. 3, e163 (2007)
  12. Kovach, M. J., Sweeney, M. T. & McCouch, S. R. New insights into the history of rice domestication. Trends Genet. 23, 578587 (2007)
  13. Sang, T. & Ge, S. The puzzle of rice domestication. J. Integr. Plant Biol. 49, 760768 (2007)
  14. Zong, Y. et al. Fire and flood management of coastal swamp enabled first rice paddy cultivation in east China. Nature 449, 459462 (2007)
  15. Fuller, D. Q. et al. The domestication process and domestication rate in rice: spikelet bases from the Lower Yangtze. Science 323, 16071610 (2009)
  16. Zhang, L. B. et al. Selection on grain shattering genes and rates of rice domestication. New Phytol. 184, 708720 (2009)
  17. Molina, J. et al. Molecular evidence for a single evolutionary origin of domesticated rice. Proc. Natl Acad. Sci. USA 108, 83518356 (2011)
  18. He, Z. et al. Two evolutionary histories in the genome of rice: the roles of domestication genes. PLoS Genet. 7, e1002100 (2011)
  19. Xu, X. et al. Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nature Biotechnol. 30, 105111 (2012)
  20. Ma, J. & Bennetzen, J. L. Rapid recent growth and divergence of rice nuclear genomes. Proc. Natl Acad. Sci. USA 101, 1240412410 (2004)
  21. Huang, X. et al. Genome-wide association studies of 14 agronomic traits in rice landraces. Nature Genet. 42, 961967 (2010)
  22. Huang, X. et al. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nature Genet. 44, 3239 (2012)
  23. Ge, S., Sang, T., Lu, B. R. & Hong, D. Y. Phylogeny of rice genomes with emphasis on origins of allotetraploid species. Proc. Natl Acad. Sci. USA 96, 1440014405 (1999)
  24. Vaughan, D. A., Morishima, H. & Kadowaki, K. Diversity in the Oryza genus. Curr. Opin. Plant Biol. 6, 139146 (2003)
  25. Doebley, J. F., Gaut, B. S. & Smith, B. D. The molecular genetics of crop domestication. Cell 127, 13091321 (2006)
  26. Novembre, J. & Stephens, M. Interpreting principal component analyses of spatial population genetic variation. Nature Genet. 40, 646649 (2008)
  27. Mizuta, Y., Harushima, Y. & Kurata, N. Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes. Proc. Natl Acad. Sci. USA 107, 2041720422 (2010)
  28. Tadege, M. et al. Reciprocal control of flowering time by OsSOC1 in transgenic Arabidopsis and by FLC in transgenic rice. Plant Biotechnol. J. 1, 361369 (2003)
  29. Wang, L. et al. Mapping 49 quantitative trait loci at high resolution through sequencing-based genotyping of rice recombinant inbred lines. Theor. Appl. Genet. 122, 327340 (2011)
  30. Xue, W. et al. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nature Genet. 40, 761767 (2008)
  31. Andaya, V. C. & Tai, T. H. Fine mapping of the qCTS12 locus, a major QTL for seedling cold tolerance in rice. Theor. Appl. Genet. 113, 467475 (2006)
  32. Saitoh, K., Onishi, K., Mikami, I., Thidar, K. & Sano, Y. Allelic diversification at the C (OsC1) locus of wild and cultivated rice: nucleotide changes associated with phenotypes. Genetics 168, 9971007 (2004)
  33. Fan, C. et al. GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor. Appl. Genet. 112, 11641171 (2006)
  34. Takano-Kai, N. et al. Evolutionary history of GS3, a gene conferring grain length in rice. Genetics 182, 13231334 (2009)
  35. Shomura, A. et al. Deletion in a gene associated with grain size increased yields during rice domestication. Nature Genet. 40, 10231028 (2008)
  36. Konishi, S. et al. An SNP caused loss of seed shattering during rice domestication. Science 312, 13921396 (2006)
  37. Wang, Z. Y. et al. The amylose content in rice endosperm is related to the post-transcriptional regulation of the waxy gene. Plant J. 7, 613622 (1995)
  38. 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, 283294 (2006)
  39. Sweeney, M. T. et al. Global dissemination of a single mutation conferring white pericarp in rice. PLoS Genet. 3, e133 (2007)
  40. Hernandez, R. D. A flexible forward simulator for populations subjects to selection and demography. Bioinformatics 24, 27862787 (2008)
  41. Huang, X. et al. High-throughput genotyping by whole-genome resequencing. Genome Res. 19, 10681076 (2009)
  42. Chen, K. Y., Cong, B., Wing, R., Vrebalov, J. & Tanksley, S. D. Changes in regulation of a transcription factor lead to autogamy in cultivated tomatoes. Science 318, 643645 (2007)
  43. Rieseberg, L. H. & Blackman, B. K. Speciation genes in plants. Ann. Bot. 106, 439455 (2010)
  44. Gan, X. et al. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419423 (2011)
  45. Schneeberger, K. et al. Reference-guided assembly of four diverse Arabidopsis thaliana genomes. Proc. Natl Acad. Sci. USA 108, 1024910254 (2011)
  46. Lu, T. et al. Collection and comparative analysis of 1888 full-length cDNAs from wild rice Oryza rufipogon Griff. W1943. DNA Res. 15, 285295 (2008)
  47. Tang, H., Sezen, U. & Paterson, A. H. Domestication and plant genomes. Curr. Opin. Plant Biol. 13, 160166 (2010)
  48. Morrell, P. L., Buckler, E. S. & Ross-Ibarra, J. Crop genomics: advances and applications. Nature Rev. Genet. 13, 8596 (2012)
  49. Kozarewa, I. et al. Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of (G+C)-biased genomes. Nature Methods 6, 291295 (2009)
  50. Barrett, J. C., Fry, B., Maller, J. & Daly, M. J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263265 (2005)
  51. Felsenstein, J. PHYLIP: phylogeny inference package (version 3.2). Cladistics 5, 164166 (1989)
  52. Price, A. L. et al. Principal components analysis corrects for stratification in genome-wide association studies. Nature Genet. 38, 904909 (2006)
  53. Churchill, G. A. & Doerge, R. W. Empirical threshold values for quantitative trait mapping. Genetics 138, 963971 (1994)
  54. Sabeti, P. C. et al. Genome-wide detection and characterization of positive selection in human populations. Nature 449, 913918 (2007)
  55. Zhang, Z. et al. Mixed linear model approach adapted for genome-wide association studies. Nature Genet. 42, 355360 (2010)
  56. Wang, S., Basten, C. J. & Zeng, Z. B. Windows QTL Cartographer 2.5. (Department of Statistics, North Carolina State Univ., 2007)
  57. Mullikin, J. C. & Ning, Z. The phusion assembler. Genome Res. 13, 8190 (2003)
  58. de la Bastide, M. & McCombie, W. R. Assembling genomic DNA sequences with PHRAP. Curr. Protoc. Bioinformatics 17, 11.4.111.4.15 (2007)
  59. Wu, T. D. & Watanabe, C. K. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21, 18591875 (2005)
  60. Kurtz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004)
  61. Salamov, A. A. & Solovyev, V. V. Ab initio gene finding in Drosophila genomic DNA. Genome Res. 10, 516522 (2000)
  62. Rice, P., Longden, I. & Bleasby, A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16, 276277 (2000)

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Author information

  1. These authors contributed equally to this work.

    • Xuehui Huang,
    • Nori Kurata,
    • Xinghua Wei &
    • Zi-Xuan Wang

Affiliations

  1. National Center for Gene Research, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200233, China

    • Xuehui Huang,
    • Zi-Xuan Wang,
    • Ahong Wang,
    • Qiang Zhao,
    • Yan Zhao,
    • Kunyan Liu,
    • Hengyun Lu,
    • Wenjun Li,
    • Yunli Guo,
    • Yiqi Lu,
    • Congcong Zhou,
    • Danlin Fan,
    • Qijun Weng,
    • Chuanrang Zhu,
    • Tao Huang,
    • Lei Zhang,
    • Yongchun Wang,
    • Lei Feng,
    • Qilin Zhan,
    • Canyang Li,
    • Tingting Lu,
    • Qi Feng &
    • Bin Han
  2. Plant Genetics Laboratory and Comparative Genomics Laboratory, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan

    • Nori Kurata,
    • Zi-Xuan Wang,
    • Hiroyasu Furuumi,
    • Takahiko Kubo,
    • Toshie Miyabayashi,
    • Asao Fujiyama &
    • Atsushi Toyoda
  3. State Key Laboratory of Rice Biology, China National Rice Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou 310006, China

    • Xinghua Wei,
    • Xiaoping Yuan,
    • Qun Xu,
    • Guojun Dong &
    • Qian Qian
  4. National Center for Plant Gene Research, State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China

    • Jiayang Li
  5. Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100029, China

    • Bin Han

Contributions

B.H. conceived the project and its components. X.H. and B.H. designed studies and contributed to the original concept of the project. X.W., X.Y. and Q.X. contributed the collection of rice cultivars and Chinese wild rice accessions. N.K., H.F., T.K., T.M., A.F. and A.T. contributed the collection of other wild rice accessions and analysed geographical distributions of wild rice. Z.-X.W., A.W., Y.W., L.F., Qilin Z., C.L., G.D. and Q.Q. contributed in phenotyping of rice. Z.-X.W., A.W. and L.F. contributed in phenotyping of the backcross inbred line population and genetic mapping of domestication-related traits. W.L., Y.G., Y.L., C.Z., D.F., Q.W. and Q.F. performed the genome sequencing. X.H., Y.Z., K.L., C.Z., T.H., L.Z. and T.L. performed genome data analysis. Qiang Z. and H.L. performed de novo genome assembly. X.H. performed evolutionary study and genome annotation. X.H., Y.Z. and K.L performed GWAS, population genetics, and statistical analyses. J.L. contributed to functional analyses. X.H. and B.H. analysed whole data and wrote the paper.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

DNA sequencing data are deposited in the European Nucleotide Archive (http://www.ebi.ac.uk/ena/) under accession numbers ERP001143, ERP000729 and ERP000106. De novo assembly and genome annotation of wild rice W1943, the genotype dataset of 1,529 rice accessions and the imputed dataset of 446 O. rufipogon accessions for GWAS are available at the Rice Haplotype Map Project database (http://www.ncgr.ac.cn/RiceHap3).

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