Home LiteratureArticle Details
PMID: 19506305 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Evolutionary history of GS3, a gene conferring grain length in rice.

Genetics ·Vol. 182 ·No. 4 ·2009-08-00 ·Pages 1323-34

Takano-Kai N, Jiang H, Kubo T, Sweeney M, Matsumoto T, Kanamori H, Padhukasahasram B, Bustamante C, Yoshimura A, Doi K, McCouch S

Abstract

Unlike maize and wheat, where artificial selection is associated with an almost uniform increase in seed or grain size, domesticated rice exhibits dramatic phenotypic diversity for grain size and shape. Here we clone and characterize GS3, an evolutionarily important gene controlling grain size in rice. We show that GS3 is highly expressed in young panicles in both short- and long-grained varieties but is not expressed in leaves or panicles after flowering, and we use genetic transformation to demonstrate that the dominant allele for short grain complements the long-grain phenotype. An association study revealed that a C to A mutation in the second exon of GS3 (A allele) was associated with enhanced grain length in Oryza sativa but was absent from other Oryza species. Linkage disequilibrium (LD) was elevated and there was a 95.7% reduction in nucleotide diversity (theta(pi)) across the gene in accessions carrying the A allele, suggesting positive selection for long grain. Haplotype analysis traced the origin of the long-grain allele to a Japonica-like ancestor and demonstrated introgression into the Indica gene pool. This study indicates a critical role for GS3 in defining the seed morphologies of modern subpopulations of O. sativa and enhances the potential for genetic manipulation of grain size in rice.

MeSH Terms
Alleles Base Sequence Edible Grain/genetics Evolution, Molecular Genes, Plant/genetics,physiology Haplotypes Linkage Disequilibrium Molecular Sequence Data Oryza/genetics Phenotype Seeds/genetics
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Takano-Kai Noriko
Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan.
Jiang Hui
Kubo Takahiko
Sweeney Megan
Matsumoto Takashi
Kanamori Hiroyuki
Padhukasahasram Badri
Bustamante Carlos
Yoshimura Atsushi
Doi Kazuyuki
McCouch Susan
References (50)
50 references, click to expand
  1. The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs.
    Development. 2006 Jan;133(2):251-61 PMID: 16339187
  2. Rice domestication by reducing shattering.
    Science. 2006 Mar 31;311(5769):1936-9 PMID: 16527928
  3. Control of seed mass and seed yield by the floral homeotic gene APETALA2.
    Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):3117-22 PMID: 15708974
  4. 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
  5. The OsTB1 gene negatively regulates lateral branching in rice.
    Plant J. 2003 Feb;33(3):513-20 PMID: 12581309
  6. Chloroplast DNA diversity in wild and cultivated species of rice (Genus Oryza, section Oryza). Cladistic-mutation and genetic-distance analysis.
    Theor Appl Genet. 1990 Aug;80(2):209-22 PMID: 24220898
  7. Control of seed size in plants.
    Proc Natl Acad Sci U S A. 2005 Dec 13;102(50):17887-8 PMID: 16330781
  8. Genetic structure and diversity in Oryza sativa L.
    Genetics. 2005 Mar;169(3):1631-8 PMID: 15654106
  9. Arabidopsis haiku mutants reveal new controls of seed size by endosperm.
    Plant Physiol. 2003 Apr;131(4):1661-70 PMID: 12692325
  10. Global dissemination of a single mutation conferring white pericarp in rice.
    PLoS Genet. 2007 Aug;3(8):e133 PMID: 17696613
  11. Identification of SNPs in the waxy gene among glutinous rice cultivars and their evolutionary significance during the domestication process of rice.
    Theor Appl Genet. 2004 May;108(7):1200-4 PMID: 14740088
  12. Control of seed mass by APETALA2.
    Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):3123-8 PMID: 15708976
  13. Mapping quantitative trait loci for yield, yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson.
    Theor Appl Genet. 2003 Aug;107(3):479-93 PMID: 12736777
  14. Genomic paleontology provides evidence for two distinct origins of Asian rice (Oryza sativa L.).
    Mol Genet Genomics. 2004 Dec;272(5):504-11 PMID: 15503144
  15. A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit.
    Science. 2008 Mar 14;319(5869):1527-30 PMID: 18339939
  16. Genetic differentiation for nuclear, mitochondrial and chloroplast genomes in common wild rice ( Oryza rufipogon Griff.) and cultivated rice ( Oryza sativa L.).
    Theor Appl Genet. 2002 Jun;104(8):1335-1345 PMID: 12582589
  17. von Willebrand factor type C domain-containing proteins regulate bone morphogenetic protein signaling through different recognition mechanisms.
    J Biol Chem. 2007 Jul 6;282(27):20002-14 PMID: 17483092
  18. 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
  19. Genome-wide patterns of nucleotide polymorphism in domesticated rice.
    PLoS Genet. 2007 Sep;3(9):1745-56 PMID: 17907810
  20. A novel database of disulfide patterns and its application to the discovery of distantly related homologs.
    J Mol Biol. 2004 Jan 23;335(4):1083-92 PMID: 14698301
  21. Characterization of the main effects, epistatic effects and their environmental interactions of QTLs on the genetic basis of yield traits in rice.
    Theor Appl Genet. 2002 Aug;105(2-3):248-257 PMID: 12582526
  22. New insights into the history of rice domestication.
    Trends Genet. 2007 Nov;23(11):578-87 PMID: 17963977
  23. Convergent domestication of cereal crops by independent mutations at corresponding genetic Loci.
    Science. 1995 Sep 22;269(5231):1714-8 PMID: 17821643
  24. A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase.
    Nat Genet. 2007 May;39(5):623-30 PMID: 17417637
  25. Control of early seed development.
    Annu Rev Cell Dev Biol. 2001;17:677-99 PMID: 11687501
  26. Control of rice grain-filling and yield by a gene with a potential signature of domestication.
    Nat Genet. 2008 Nov;40(11):1370-4 PMID: 18820698
  27. Arabidopsis UPF1 RNA helicase for nonsense-mediated mRNA decay is involved in seed size control and is essential for growth.
    Plant Cell Physiol. 2006 May;47(5):572-80 PMID: 16540482
  28. DnaSP, DNA polymorphism analyses by the coalescent and other methods.
    Bioinformatics. 2003 Dec 12;19(18):2496-7 PMID: 14668244
  29. 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
  30. Isozymes and classification of Asian rice varieties.
    Theor Appl Genet. 1987 May;74(1):21-30 PMID: 24241451
  31. GASA4, one of the 14-member Arabidopsis GASA family of small polypeptides, regulates flowering and seed development.
    Plant Cell Physiol. 2007 Mar;48(3):471-83 PMID: 17284469
  32. Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid.
    Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9226-31 PMID: 11038567
  33. COMPARATIVE EVOLUTION OF CEREALS.
    Evolution. 1973 Jun;27(2):311-325 PMID: 28564784
  34. Rice plant development: from zygote to spikelet.
    Plant Cell Physiol. 2005 Jan;46(1):23-47 PMID: 15659435
  35. Not just a grain of rice: the quest for quality.
    Trends Plant Sci. 2009 Mar;14(3):133-9 PMID: 19230745
  36. A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase.
    Am J Hum Genet. 2006 Apr;78(4):629-44 PMID: 16532393
  37. Natural variation in an ABC transporter gene associated with seed size evolution in tomato species.
    PLoS Genet. 2009 Jan;5(1):e1000347 PMID: 19165318
  38. SHORT HYPOCOTYL UNDER BLUE1 associates with MINISEED3 and HAIKU2 promoters in vivo to regulate Arabidopsis seed development.
    Plant Cell. 2009 Jan;21(1):106-17 PMID: 19141706
  39. Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight.
    Cell Res. 2008 Dec;18(12):1199-209 PMID: 19015668
  40. Identification of trait-improving quantitative trait loci alleles from a wild rice relative, Oryza rufipogon.
    Genetics. 1998 Oct;150(2):899-909 PMID: 9755218
  41. Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana.
    Genes Dev. 2008 May 15;22(10):1331-6 PMID: 18483219
  42. Deletion in a gene associated with grain size increased yields during rice domestication.
    Nat Genet. 2008 Aug;40(8):1023-8 PMID: 18604208
  43. QTL mapping and introgression of yield-related traits from Oryza glumaepatula to cultivated rice ( Oryza sativa) using microsatellite markers.
    Theor Appl Genet. 2002 May;104(6-7):1192-1203 PMID: 12582630
  44. Evolutionary relationships in the Sativa group of Oryza based on isozyme data.
    Genet Sel Evol. 1985;17(1):89-114 PMID: 22879188
  45. Fine mapping of a grain-weight quantitative trait locus in the pericentromeric region of rice chromosome 3.
    Genetics. 2004 Dec;168(4):2187-95 PMID: 15611185
  46. Genome plasticity a key factor in the success of polyploid wheat under domestication.
    Science. 2007 Jun 29;316(5833):1862-6 PMID: 17600208
  47. Inference of population structure using multilocus genotype data.
    Genetics. 2000 Jun;155(2):945-59 PMID: 10835412
  48. Epistasis for three grain yield components in rice (Oryza sativa L.).
    Genetics. 1997 Feb;145(2):453-65 PMID: 9071598
  49. Gramene QTL database: development, content and applications.
    Database (Oxford). 2009;2009:bap005 PMID: 20157478
  50. 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. 2006 Apr;112(6):1164-71 PMID: 16453132
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
1943-2631
DOI
10.1534/genetics.109.103002
Published
2009-08-00
Epub
2009-00-08
Pages
1323-34
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC2728869
Subset
IM
Databases
GENBANK
AB488612, AB488613, AB488614, AB488615, AB488616, AB488617, AB488618, AB488619, AB488620, AB488621, AB488622, AB488623, AB488624, AB488625, AB488626, AB488627, AB488628, AB488629, AB488630, AB488631, AB488632, AB488633, AB488634, AB488635, AB488636, AB488637, AB488638, AB488639, AB488640, AB488641, AB488642, AB488643, AB488644, AB488645, AB488646, AB488647, AB488648, AB488649, AB488650, AB488651, AB488652, AB488653, AB488654, AB488655, AB488656, AB488657, AB488658, AB488659, AB488660, AB488661, AB488662, AB488663, AB488664, AB488665
External Links
PubMed source DOI: 10.1534/genetics.109.103002 PMC Full Text View journal details
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]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2