Home LiteratureArticle Details
PMID: 17112320 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Genomic variation in rice: genesis of highly polymorphic linkage blocks during domestication.

PLoS genetics ·Vol. 2 ·No. 11 ·2006-11-17 ·Pages e199

Tang T, Lu J, Huang J, He J, McCouch SR, Shen Y, Kai Z, Purugganan MD, Shi S, Wu CI

Abstract

Genomic regions that are unusually divergent between closely related species or racial groups can be particularly informative about the process of speciation or the operation of natural selection. The two sequenced genomes of cultivated Asian rice, Oryza sativa, reveal that at least 6% of the genomes are unusually divergent. Sequencing of ten unlinked loci from the highly divergent regions consistently identified two highly divergent haplotypes with each locus in nearly complete linkage disequilibrium among 25 O. sativa cultivars and 35 lines from six wild species. The existence of two highly divergent haplotypes in high divergence regions in species from all geographical areas (Africa, Asia, and Oceania) was in contrast to the low polymorphism and low linkage disequilibrium that were observed in other parts of the genome, represented by ten reference loci. While several natural processes are likely to contribute to this pattern of genomic variation, domestication may have greatly exaggerated the trend. In this hypothesis, divergent haplotypes that were adapted to different geographical and ecological environments migrated along with humans during the development of domesticated varieties. If true, these high divergence regions of the genome would be enriched for loci that contribute to the enormous range of phenotypic variation observed among domesticated breeds.

MeSH Terms
Agriculture Base Sequence Crops, Agricultural/genetics Genes, Plant/genetics Genome, Plant/genetics Haplotypes Linkage Disequilibrium/genetics Molecular Sequence Data Oryza/genetics Phylogeny Polymorphism, Genetic Population Dynamics Species Specificity
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Tang Tian
State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen (Zhongshan) University, Guangzhou, People's Republic of China.
Lu Jian
Huang Jianzi
He Jinghong
McCouch Susan R
Shen Yang
Kai Zeng
Purugganan Michael D
Shi Suhua
Wu Chung-I
Conflict of Interest

Competing interests. The authors have declared that no competing interests exist.

References (49)
49 references, click to expand
  1. The limits of selection during maize domestication.
    Nature. 1999 Mar 18;398(6724):236-9 PMID: 10094045
  2. Evolutionary genetics of self-incompatibility in the Solanaceae.
    Plant Mol Biol. 2000 Jan;42(1):169-79 PMID: 10688135
  3. MEGA2: molecular evolutionary genetics analysis software.
    Bioinformatics. 2001 Dec;17(12):1244-5 PMID: 11751241
  4. Recombination, balancing selection and phylogenies in MHC and self-incompatibility genes.
    Genetics. 2001 Dec;159(4):1833-44 PMID: 11779818
  5. Diverse variation of reproductive barriers in three intraspecific rice crosses.
    Genetics. 2002 Jan;160(1):313-22 PMID: 11805066
  6. A draft sequence of the rice genome (Oryza sativa L. ssp. indica).
    Science. 2002 Apr 5;296(5565):79-92 PMID: 11935017
  7. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica).
    Science. 2002 Apr 5;296(5565):92-100 PMID: 11935018
  8. Genetic diversity and selection in the maize starch pathway.
    Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):12959-62 PMID: 12244216
  9. Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation.
    Evolution. 2003 Mar;57(3):447-59 PMID: 12703935
  10. Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice.
    Science. 2003 Jul 18;301(5631):376-9 PMID: 12869764
  11. The dog genome: survey sequencing and comparative analysis.
    Science. 2003 Sep 26;301(5641):1898-903 PMID: 14512627
  12. MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years?
    J Evol Biol. 2003 May;16(3):363-77 PMID: 14635837
  13. DnaSP, DNA polymorphism analyses by the coalescent and other methods.
    Bioinformatics. 2003 Dec 12;19(18):2496-7 PMID: 14668244
  14. Genes and speciation.
    Nat Rev Genet. 2004 Feb;5(2):114-22 PMID: 14735122
  15. High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal.
    Proc Natl Acad Sci U S A. 2004 Mar 9;101(10):3490-4 PMID: 14990802
  16. The genetic, developmental, and molecular bases of fruit size and shape variation in tomato.
    Plant Cell. 2004;16 Suppl:S181-9 PMID: 15131251
  17. Rapid recent growth and divergence of rice nuclear genomes.
    Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12404-10 PMID: 15240870
  18. Pattern of polymorphism after strong artificial selection in a domestication event.
    Proc Natl Acad Sci U S A. 2004 Jul 20;101(29):10667-72 PMID: 15249682
  19. Haploview: analysis and visualization of LD and haplotype maps.
    Bioinformatics. 2005 Jan 15;21(2):263-5 PMID: 15297300
  20. Population history and natural selection shape patterns of genetic variation in 132 genes.
    PLoS Biol. 2004 Oct;2(10):e286 PMID: 15361935
  21. The population structure of African cultivated rice oryza glaberrima (Steud.): evidence for elevated levels of linkage disequilibrium caused by admixture with O. sativa and ecological adaptation.
    Genetics. 2005 Mar;169(3):1639-47 PMID: 15545652
  22. A draft sequence for the genome of the domesticated silkworm (Bombyx mori).
    Science. 2004 Dec 10;306(5703):1937-40 PMID: 15591204
  23. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution.
    Nature. 2004 Dec 9;432(7018):695-716 PMID: 15592404
  24. Genetic structure and diversity in Oryza sativa L.
    Genetics. 2005 Mar;169(3):1631-8 PMID: 15654106
  25. Inferring the mode of speciation from genomic data: a study of the great apes.
    Genetics. 2005 Jan;169(1):259-64 PMID: 15677748
  26. The Genomes of Oryza sativa: a history of duplications.
    PLoS Biol. 2005 Feb;3(2):e38 PMID: 15685292
  27. High-diversity genes in the Arabidopsis genome.
    Genetics. 2005 Aug;170(4):1897-911 PMID: 15911589
  28. Balancing selection in the wild: testing population genetics theory of self-incompatibility in the rare species Brassica insularis.
    Genetics. 2005 Sep;171(1):279-89 PMID: 15944365
  29. Phylogenetic relationships among A-genome species of the genus Oryza revealed by intron sequences of four nuclear genes.
    New Phytol. 2005 Jul;167(1):249-65 PMID: 15948847
  30. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks.
    Bioinformatics. 2005 Aug 15;21(16):3448-9 PMID: 15972284
  31. The Oryza bacterial artificial chromosome library resource: construction and analysis of 12 deep-coverage large-insert BAC libraries that represent the 10 genome types of the genus Oryza.
    Genome Res. 2006 Jan;16(1):140-7 PMID: 16344555
  32. The accumulation of deleterious mutations in rice genomes: a hypothesis on the cost of domestication.
    Trends Genet. 2006 Mar;22(3):126-31 PMID: 16443304
  33. Genetic analysis of rice domestication syndrome with the wild annual species, Oryza nivara.
    New Phytol. 2006;170(1):185-93 PMID: 16539615
  34. Balancing selection and its effects on sequences in nearby genome regions.
    PLoS Genet. 2006 Apr;2(4):e64 PMID: 16683038
  35. Genetic evidence for complex speciation of humans and chimpanzees.
    Nature. 2006 Jun 29;441(7097):1103-8 PMID: 16710306
  36. Scan of human genome reveals no new Loci under ancient balancing selection.
    Genetics. 2006 Aug;173(4):2165-77 PMID: 16751668
  37. Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa.
    Proc Natl Acad Sci U S A. 2006 Jun 20;103(25):9578-83 PMID: 16766658
  38. Genetic diversity and differentiation of indica and japonica rice detected by RFLP analysis.
    Theor Appl Genet. 1992 Feb;83(4):495-9 PMID: 24202597
  39. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
    Genetics. 1989 Nov;123(3):585-95 PMID: 2513255
  40. INTROGRESSION ACROSS ISOLATING BARRIERS IN WILD AND CULTIVATED ORYZA SPECIES.
    Evolution. 1970 Jun;24(2):344-355 PMID: 28565062
  41. USING HITCHHIKING GENES TO STUDY ADAPTATION AND DIVERGENCE DURING SPECIATION WITHIN THE DROSOPHILA MELANOGASTER SPECIES COMPLEX.
    Evolution. 1994 Dec;48(6):1900-1913 PMID: 28565154
  42. The neighbor-joining method: a new method for reconstructing phylogenetic trees.
    Mol Biol Evol. 1987 Jul;4(4):406-25 PMID: 3447015
  43. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.
    J Mol Evol. 1980 Dec;16(2):111-20 PMID: 7463489
  44. Unbiased estimation of the rates of synonymous and nonsynonymous substitution.
    J Mol Evol. 1993 Jan;36(1):96-9 PMID: 8433381
  45. A coalescent estimator of the population recombination rate.
    Genetics. 1997 Mar;145(3):833-46 PMID: 9055092
  46. Seed banks and molecular maps: unlocking genetic potential from the wild.
    Science. 1997 Aug 22;277(5329):1063-6 PMID: 9262467
  47. Strong balancing selection at HLA loci: evidence from segregation in South Amerindian families.
    Proc Natl Acad Sci U S A. 1997 Nov 11;94(23):12452-6 PMID: 9356470
  48. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  49. A high-density rice genetic linkage map with 2275 markers using a single F2 population.
    Genetics. 1998 Jan;148(1):479-94 PMID: 9475757
Article Info
Journal
PLoS genetics
Abbr.
PLoS Genet
ISSN
1553-7404
DOI
10.1371/journal.pgen.0020199
Published
2006-11-17
Pages
e199
Language
English
Region
United States
NLM ID
101239074
PMCID
PMC1636696
Subset
IM
Databases
GENBANK
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PubMed source DOI: 10.1371/journal.pgen.0020199 PMC Full Text View journal details
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