Home LiteratureArticle Details
PMID: 15685292 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

The Genomes of Oryza sativa: a history of duplications.

PLoS biology ·Vol. 3 ·No. 2 ·2005-02-00 ·Pages e38

Yu J, Wang J, Lin W, Li S, Li H, Zhou J, Ni P, Dong W, Hu S, Zeng C, Zhang J, Zhang Y, Li R, Xu Z, Li S, Li X, Zheng H, Cong L, Lin L, Yin J, Geng J, Li G, Shi J, Liu J, Lv H, Li J, Wang J, Deng Y, Ran L, Shi X, Wang X, Wu Q, Li C, Ren X, Wang J, Wang X, Li D, Liu D, Zhang X, Ji Z, Zhao W, Sun Y, Zhang Z, Bao J, Han Y, Dong L, Ji J, Chen P, Wu S, Liu J, Xiao Y, Bu D, Tan J, Yang L, Ye C, Zhang J, Xu J, Zhou Y, Yu Y, Zhang B, Zhuang S, Wei H, Liu B, Lei M, Yu H, Li Y, Xu H, Wei S, He X, Fang L, Zhang Z, Zhang Y, Huang X, Su Z, Tong W, Li J, Tong Z, Li S, Ye J, Wang L, Fang L, Lei T, Chen C, Chen H, Xu Z, Li H, Huang H, Zhang F, Xu H, Li N, Zhao C, Li S, Dong L, Huang Y, Li L, Xi Y, Qi Q, Li W, Zhang B, Hu W, Zhang Y, Tian X, Jiao Y, Liang X, Jin J, Gao L, Zheng W, Hao B, Liu S, Wang W, Yuan L, Cao M, McDermott J, Samudrala R, Wang J, Wong GK, Yang H

Abstract

We report improved whole-genome shotgun sequences for the genomes of indica and japonica rice, both with multimegabase contiguity, or almost 1,000-fold improvement over the drafts of 2002. Tested against a nonredundant collection of 19,079 full-length cDNAs, 97.7% of the genes are aligned, without fragmentation, to the mapped super-scaffolds of one or the other genome. We introduce a gene identification procedure for plants that does not rely on similarity to known genes to remove erroneous predictions resulting from transposable elements. Using the available EST data to adjust for residual errors in the predictions, the estimated gene count is at least 38,000-40,000. Only 2%-3% of the genes are unique to any one subspecies, comparable to the amount of sequence that might still be missing. Despite this lack of variation in gene content, there is enormous variation in the intergenic regions. At least a quarter of the two sequences could not be aligned, and where they could be aligned, single nucleotide polymorphism (SNP) rates varied from as little as 3.0 SNP/kb in the coding regions to 27.6 SNP/kb in the transposable elements. A more inclusive new approach for analyzing duplication history is introduced here. It reveals an ancient whole-genome duplication, a recent segmental duplication on Chromosomes 11 and 12, and massive ongoing individual gene duplications. We find 18 distinct pairs of duplicated segments that cover 65.7% of the genome; 17 of these pairs date back to a common time before the divergence of the grasses. More important, ongoing individual gene duplications provide a never-ending source of raw material for gene genesis and are major contributors to the differences between members of the grass family.

MeSH Terms
Base Sequence China Chromosome Mapping Gene Duplication Genes, Plant Genome, Plant Oryza/genetics
Authors & Affiliations
117 authors, click to expand affiliations / ORCID
Yu Jun
Beijing Institute of Genomics of the Chinese Academy of Sciences, Beijing Genomics Institute, Beijing Proteomics Institute, China. [email protected] <[email protected]>
Wang Jun
Lin Wei
Li Songgang
Li Heng
Zhou Jun
Ni Peixiang
Dong Wei
Hu Songnian
Zeng Changqing
Zhang Jianguo
Zhang Yong
Li Ruiqiang
Xu Zuyuan
Li Shengting
Li Xianran
Zheng Hongkun
Cong Lijuan
Lin Liang
Yin Jianning
Geng Jianing
Li Guangyuan
Shi Jianping
Liu Juan
Lv Hong
Li Jun
Wang Jing
Deng Yajun
Ran Longhua
Shi Xiaoli
Wang Xiyin
Wu Qingfa
Li Changfeng
Ren Xiaoyu
Wang Jingqiang
Wang Xiaoling
Li Dawei
Liu Dongyuan
Zhang Xiaowei
Ji Zhendong
Zhao Wenming
Sun Yongqiao
Zhang Zhenpeng
Bao Jingyue
Han Yujun
Dong Lingli
Ji Jia
Chen Peng
Wu Shuming
Liu Jinsong
Xiao Ying
Bu Dongbo
Tan Jianlong
Yang Li
Ye Chen
Zhang Jingfen
Xu Jingyi
Zhou Yan
Yu Yingpu
Zhang Bing
Zhuang Shulin
Wei Haibin
Liu Bin
Lei Meng
Yu Hong
Li Yuanzhe
Xu Hao
Wei Shulin
He Ximiao
Fang Lijun
Zhang Zengjin
Zhang Yunze
Huang Xiangang
Su Zhixi
Tong Wei
Li Jinhong
Tong Zongzhong
Li Shuangli
Ye Jia
Wang Lishun
Fang Lin
Lei Tingting
Chen Chen
Chen Huan
Xu Zhao
Li Haihong
Huang Haiyan
Zhang Feng
Xu Huayong
Li Na
Zhao Caifeng
Li Shuting
Dong Lijun
Huang Yanqing
Li Long
Xi Yan
Qi Qiuhui
Li Wenjie
Zhang Bo
Hu Wei
Zhang Yanling
Tian Xiangjun
Jiao Yongzhi
Liang Xiaohu
Jin Jiao
Gao Lei
Zheng Weimou
Hao Bailin
Liu Siqi
Wang Wen
Yuan Longping
Cao Mengliang
McDermott Jason
Samudrala Ram
Wang Jian
Wong Gane Ka-Shu
Yang Huanming
References (84)
84 references, click to expand
  1. Comparative sequence analysis of plant nuclear genomes:m microcolinearity and its many exceptions.
    Plant Cell. 2000 Jul;12(7):1021-9 PMID: 10899971
  2. The InterPro Database, 2003 brings increased coverage and new features.
    Nucleic Acids Res. 2003 Jan 1;31(1):315-8 PMID: 12520011
  3. The role of genetic and genomic attributes in the success of polyploids.
    Proc Natl Acad Sci U S A. 2000 Jun 20;97(13):7051-7 PMID: 10860970
  4. Yesterday's polyploids and the mystery of diploidization.
    Nat Rev Genet. 2001 May;2(5):333-41 PMID: 11331899
  5. Molecular evidence for an ancient duplication of the entire yeast genome.
    Nature. 1997 Jun 12;387(6634):708-13 PMID: 9192896
  6. BLAT--the BLAST-like alignment tool.
    Genome Res. 2002 Apr;12(4):656-64 PMID: 11932250
  7. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution.
    Plant Cell. 2004 Jul;16(7):1679-91 PMID: 15208398
  8. DNA sequence evidence for the segmental allotetraploid origin of maize.
    Proc Natl Acad Sci U S A. 1997 Jun 24;94(13):6809-14 PMID: 11038553
  9. Obtaining the sequence of the rice genome and lessons learned along the way.
    Trends Plant Sci. 2002 Dec;7(12):538-42 PMID: 12475494
  10. Consistent over-estimation of gene number in complex plant genomes.
    Curr Opin Plant Biol. 2004 Dec;7(6):732-6 PMID: 15491923
  11. Mega-introns in the dynein gene DhDhc7(Y) on the heterochromatic Y chromosome give rise to the giant threads loops in primary spermatocytes of Drosophila hydei.
    Genetics. 2000 Feb;154(2):759-69 PMID: 10655227
  12. How can we deliver the large plant genomes? Strategies and perspectives.
    Curr Opin Plant Biol. 2002 Apr;5(2):173-7 PMID: 11856615
  13. On the importance of being finished.
    Genome Biol. 2002 Sep 27;3(10):COMMENT2010 PMID: 12372139
  14. The hidden duplication past of Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13627-32 PMID: 12374856
  15. An evolutionary analysis of orphan genes in Drosophila.
    Genome Res. 2003 Oct;13(10):2213-9 PMID: 14525923
  16. Evolution of genes and taxa: a primer.
    Plant Mol Biol. 2000 Jan;42(1):1-23 PMID: 10688128
  17. Assessing sequence comparison methods with reliable structurally identified distant evolutionary relationships.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):6073-8 PMID: 9600919
  18. The genetic colinearity of rice and other cereals on the basis of genomic sequence analysis.
    Curr Opin Plant Biol. 2003 Apr;6(2):128-33 PMID: 12667868
  19. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica).
    Science. 2002 Apr 5;296(5565):92-100 PMID: 11935018
  20. The phusion assembler.
    Genome Res. 2003 Jan;13(1):81-90 PMID: 12529309
  21. Annotation transfer between genomes: protein-protein interologs and protein-DNA regulogs.
    Genome Res. 2004 Jun;14(6):1107-18 PMID: 15173116
  22. Current status of the sequence of the rice genome and prospects for finishing the first monocot genome.
    Plant Physiol. 2002 Dec;130(4):1585-6 PMID: 12481040
  23. Sequence and analysis of rice chromosome 4.
    Nature. 2002 Nov 21;420(6913):316-20 PMID: 12447439
  24. Evolutionary history of the grasses.
    Plant Physiol. 2001 Mar;125(3):1198-205 PMID: 11244101
  25. Plant genome archaeology: evidence for conserved ancestral chromosome segments in dicotyledonous plant species.
    Plant Biotechnol J. 2003 Mar;1(2):91-9 PMID: 17147746
  26. Comparative genetics in the grasses.
    Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):1971-4 PMID: 9482816
  27. A draft sequence of the rice genome (Oryza sativa L. ssp. indica).
    Science. 2002 Apr 5;296(5565):79-92 PMID: 11935017
  28. The Gene Ontology Annotation (GOA) project: implementation of GO in SWISS-PROT, TrEMBL, and InterPro.
    Genome Res. 2003 Apr;13(4):662-72 PMID: 12654719
  29. BGI-RIS: an integrated information resource and comparative analysis workbench for rice genomics.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D377-82 PMID: 14681438
  30. The maps. Clone by clone by clone.
    Nature. 2001 Feb 15;409(6822):816-8 PMID: 11236993
  31. Activation of CDK-activating kinase is dependent on interaction with H-type cyclins in plants.
    Plant J. 2000 Oct;24(1):11-20 PMID: 11029700
  32. Gramene, a tool for grass genomics.
    Plant Physiol. 2002 Dec;130(4):1606-13 PMID: 12481044
  33. Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice.
    Science. 2003 Jul 18;301(5631):376-9 PMID: 12869764
  34. Lethality and centrality in protein networks.
    Nature. 2001 May 3;411(6833):41-2 PMID: 11333967
  35. A whole-genome assembly of Drosophila.
    Science. 2000 Mar 24;287(5461):2196-204 PMID: 10731133
  36. The genome sequence and structure of rice chromosome 1.
    Nature. 2002 Nov 21;420(6913):312-6 PMID: 12447438
  37. Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice.
    Genome Res. 2004 May;14(5):860-9 PMID: 15078861
  38. Rice transposable elements: a survey of 73,000 sequence-tagged-connectors.
    Genome Res. 2000 Jul;10(7):982-90 PMID: 10899147
  39. A high-density rice genetic linkage map with 2275 markers using a single F2 population.
    Genetics. 1998 Jan;148(1):479-94 PMID: 9475757
  40. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes.
    Plant Cell. 2004 Jul;16(7):1667-78 PMID: 15208399
  41. Rice as a model for comparative genomics of plants.
    Annu Rev Plant Biol. 2002;53:399-419 PMID: 12221982
  42. Towards an accurate sequence of the rice genome.
    Curr Opin Plant Biol. 2003 Apr;6(2):101-5 PMID: 12667864
  43. DIP, the Database of Interacting Proteins: a research tool for studying cellular networks of protein interactions.
    Nucleic Acids Res. 2002 Jan 1;30(1):303-5 PMID: 11752321
  44. Vertebrate gene predictions and the problem of large genes.
    Nat Rev Genet. 2003 Sep;4(9):741-9 PMID: 12951575
  45. GeneWise and Genomewise.
    Genome Res. 2004 May;14(5):988-95 PMID: 15123596
  46. Development of genome-wide DNA polymorphism database for map-based cloning of rice genes.
    Plant Physiol. 2004 Jul;135(3):1198-205 PMID: 15266053
  47. The origins of genomic duplications in Arabidopsis.
    Science. 2000 Dec 15;290(5499):2114-7 PMID: 11118139
  48. In-depth view of structure, activity, and evolution of rice chromosome 10.
    Science. 2003 Jun 6;300(5625):1566-9 PMID: 12791992
  49. Why finishing the rice genome matters.
    Science. 2002 Apr 5;296(5565):45 PMID: 11962488
  50. Prediction of complete gene structures in human genomic DNA.
    J Mol Biol. 1997 Apr 25;268(1):78-94 PMID: 9149143
  51. New in silico insight into the synteny between rice (Oryza sativa L.) and maize (Zea mays L.) highlights reshuffling and identifies new duplications in the rice genome.
    Plant J. 2004 May;38(3):396-409 PMID: 15086801
  52. K-Estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals.
    Bioinformatics. 1999 Sep;15(9):763-4 PMID: 10498777
  53. Initial sequencing and comparative analysis of the mouse genome.
    Nature. 2002 Dec 5;420(6915):520-62 PMID: 12466850
  54. Gene enrichment in plant genomic shotgun libraries.
    Curr Opin Plant Biol. 2003 Apr;6(2):150-6 PMID: 12667872
  55. Development and mapping of SSR markers for maize.
    Plant Mol Biol. 2002 Mar-Apr;48(5-6):463-81 PMID: 12004892
  56. Splitting pairs: the diverging fates of duplicated genes.
    Nat Rev Genet. 2002 Nov;3(11):827-37 PMID: 12415313
  57. The rice genome. Opening the door to comparative plant biology.
    Science. 2002 Apr 5;296(5565):60-3 PMID: 11935009
  58. Understanding mechanisms of novel gene expression in polyploids.
    Trends Genet. 2003 Mar;19(3):141-7 PMID: 12615008
  59. The evolutionary fate and consequences of duplicate genes.
    Science. 2000 Nov 10;290(5494):1151-5 PMID: 11073452
  60. Comparative genomics in the grass family: molecular characterization of grass genome structure and evolution.
    Ann Bot. 2002 Jan;89(1):3-10 PMID: 12096816
  61. An SNP map of the human genome generated by reduced representation shotgun sequencing.
    Nature. 2000 Sep 28;407(6803):513-6 PMID: 11029002
  62. Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics.
    Proc Natl Acad Sci U S A. 2004 Jun 29;101(26):9903-8 PMID: 15161969
  63. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):796-815 PMID: 11130711
  64. What happens to genes in duplicated genomes.
    Proc Natl Acad Sci U S A. 2003 Apr 15;100(8):4369-71 PMID: 12682287
  65. Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL.
    Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10274-9 PMID: 8816790
  66. The Protein Data Bank and structural genomics.
    Nucleic Acids Res. 2003 Jan 1;31(1):489-91 PMID: 12520059
  67. Ab initio gene finding in Drosophila genomic DNA.
    Genome Res. 2000 Apr;10(4):516-22 PMID: 10779491
  68. Genomic mapping by fingerprinting random clones: a mathematical analysis.
    Genomics. 1988 Apr;2(3):231-9 PMID: 3294162
  69. Extensive duplication and reshuffling in the Arabidopsis genome.
    Plant Cell. 2000 Jul;12(7):1093-101 PMID: 10899976
  70. Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and other angiosperm lineages.
    J Mol Evol. 1999 May;48(5):597-604 PMID: 10198125
  71. A statistical approach designed for finding mathematically defined repeats in shotgun data and determining the length distribution of clone-inserts.
    Genomics Proteomics Bioinformatics. 2003 Feb;1(1):43-51 PMID: 15626332
  72. Evidence that rice and other cereals are ancient aneuploids.
    Plant Cell. 2003 Sep;15(9):2192-202 PMID: 12953120
  73. RePS: a sequence assembler that masks exact repeats identified from the shotgun data.
    Genome Res. 2002 May;12(5):824-31 PMID: 11997349
  74. Impact of the presence of paralogs on sequence divergence in a set of mouse-human orthologs.
    Genome Res. 2002 Sep;12(9):1370-6 PMID: 12213774
  75. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models.
    Mol Biol Evol. 2000 Jan;17(1):32-43 PMID: 10666704
  76. Re-evaluating the relevance of ancestral shared synteny as a tool for crop improvement.
    Curr Opin Plant Biol. 2004 Apr;7(2):126-31 PMID: 15003211
  77. Rice genomes: a grainy view of future evolutionary research.
    Curr Biol. 2002 Jul 9;12(13):R470-1 PMID: 12121641
  78. An integrated physical and genetic map of the rice genome.
    Plant Cell. 2002 Mar;14(3):537-45 PMID: 11910002
  79. Bioverse: Functional, structural and contextual annotation of proteins and proteomes.
    Nucleic Acids Res. 2003 Jul 1;31(13):3736-7 PMID: 12824406
  80. The impact of polyploidy on grass genome evolution.
    Plant Physiol. 2002 Dec;130(4):1587-93 PMID: 12481041
  81. Genome evolution in polyploids.
    Plant Mol Biol. 2000 Jan;42(1):225-49 PMID: 10688139
  82. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events.
    Nature. 2003 Mar 27;422(6930):433-8 PMID: 12660784
  83. Identification of the duplicated segments in rice chromosomes 1 and 5 by linkage analysis of cDNA markers of known functions.
    Theor Appl Genet. 1994 Aug;88(6-7):722-6 PMID: 24186168
  84. Enhanced functional information from predicted protein networks.
    Trends Biotechnol. 2004 Feb;22(2):60-2; discussion 62-3 PMID: 14757037
Article Info
Journal
PLoS biology
Abbr.
PLoS Biol
ISSN
1545-7885
Published
2005-02-00
Epub
2005-00-01
Pages
e38
Language
English
Region
United States
NLM ID
101183755
PMCID
PMC546038
Subset
IM
Grants
NHGRI NIH HHS · P50 HG002351 · United States
NHGRI NIH HHS · 1 P50 HG02351 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]