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Genomic diversity and introgression in O. sativa reveal the impact of domestication and breeding on the rice genome.

Zhao K, Wright M, Kimball J, Eizenga G, McClung A, Kovach M, Tyagi W, Ali ML, Tung CW, Reynolds A, Bustamante CD, McCouch SR - PLoS ONE (2010)

Bottom Line: Our introgression analysis shows that most accessions exhibit some degree of admixture, with many individuals within a population sharing the same introgressed segment due to artificial selection.Admixture mapping and association analysis of amylose content and grain length illustrate the potential for dissecting the genetic basis of complex traits in domesticated plant populations.These analyses highlight the power of population genomics in agricultural systems to identify functionally important regions of the genome and to decipher the role of human-directed breeding in refashioning the genomes of a domesticated species.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Statistics and Computational Biology, Cornell University, Ithaca, New York, USA.

ABSTRACT

Background: The domestication of Asian rice (Oryza sativa) was a complex process punctuated by episodes of introgressive hybridization among and between subpopulations. Deep genetic divergence between the two main varietal groups (Indica and Japonica) suggests domestication from at least two distinct wild populations. However, genetic uniformity surrounding key domestication genes across divergent subpopulations suggests cultural exchange of genetic material among ancient farmers.

Methodology/principal findings: In this study, we utilize a novel 1,536 SNP panel genotyped across 395 diverse accessions of O. sativa to study genome-wide patterns of polymorphism, to characterize population structure, and to infer the introgression history of domesticated Asian rice. Our population structure analyses support the existence of five major subpopulations (indica, aus, tropical japonica, temperate japonica and GroupV) consistent with previous analyses. Our introgression analysis shows that most accessions exhibit some degree of admixture, with many individuals within a population sharing the same introgressed segment due to artificial selection. Admixture mapping and association analysis of amylose content and grain length illustrate the potential for dissecting the genetic basis of complex traits in domesticated plant populations.

Conclusions/significance: Genes in these regions control a myriad of traits including plant stature, blast resistance, and amylose content. These analyses highlight the power of population genomics in agricultural systems to identify functionally important regions of the genome and to decipher the role of human-directed breeding in refashioning the genomes of a domesticated species.

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Regions of introgression from temperate japonica into indica aligned with admixture mapping and association mapping p-values for amylose content.Genome position of SNPs and introgressions indicated across the bottom; vertical grey lines indicate chromosomes; position of Waxy gene on chromosome 6 shown as vertical dashed line. (A) Horizontal grey lines indicate accessions; blue-colored regions represent introgressions (defined by ≥5 SNPs) from temperate japonica into indica; variety names (on left) colored dark blue indicate indica accessions carrying a waxy allele introgressed from temperate japonica; those without waxy introgression indicated in red. (B) Admixture mapping p-values for amylose content using the temperate japonica component in the admixed subpopulation. (C) Association mapping p-values for amylose content in all accessions using mixed model approach. Horizontal dotted lines in both (B) and (C) represent significance values of 0.05 after Bonferroni correction.
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pone-0010780-g004: Regions of introgression from temperate japonica into indica aligned with admixture mapping and association mapping p-values for amylose content.Genome position of SNPs and introgressions indicated across the bottom; vertical grey lines indicate chromosomes; position of Waxy gene on chromosome 6 shown as vertical dashed line. (A) Horizontal grey lines indicate accessions; blue-colored regions represent introgressions (defined by ≥5 SNPs) from temperate japonica into indica; variety names (on left) colored dark blue indicate indica accessions carrying a waxy allele introgressed from temperate japonica; those without waxy introgression indicated in red. (B) Admixture mapping p-values for amylose content using the temperate japonica component in the admixed subpopulation. (C) Association mapping p-values for amylose content in all accessions using mixed model approach. Horizontal dotted lines in both (B) and (C) represent significance values of 0.05 after Bonferroni correction.

Mentions: The glutinous phenotype of rice is largely controlled by the Waxy (Wx) gene, located at 1.7 Mb on the short arm of chromosome 6. Waxy is a granule-bound starch synthase that is responsible for amylose biosynthesis in the grain [65]. There are two major functional haplotype groups of Wx that differentiate the Indica and Japonica rice varietal groups, with Wxa found mostly in Indica and Wxb mostly in Japonica. The amylose content is significantly lower in the Wxb haplotype [66]. In our study, the indica varieties Ming Hui, Sundensis, IR-44595, 93-11, Yang Dao 6, and Minghui 63 have a temperate japonica introgression at the Wx locus (Figure 4A). A SNP at the functional G/T mutation in intron 1 that is indicative of the Wxb haplotype [67] was included on our GoldenGate assay and our genotyping results confirmed that all of the indica varieties carrying the introgression marked by the T-allele have significantly lower amylose content (all less than 18.5% with mean = 14.1%) than those carrying the G-allele (all no less than 20% with mean = 23.6%).


Genomic diversity and introgression in O. sativa reveal the impact of domestication and breeding on the rice genome.

Zhao K, Wright M, Kimball J, Eizenga G, McClung A, Kovach M, Tyagi W, Ali ML, Tung CW, Reynolds A, Bustamante CD, McCouch SR - PLoS ONE (2010)

Regions of introgression from temperate japonica into indica aligned with admixture mapping and association mapping p-values for amylose content.Genome position of SNPs and introgressions indicated across the bottom; vertical grey lines indicate chromosomes; position of Waxy gene on chromosome 6 shown as vertical dashed line. (A) Horizontal grey lines indicate accessions; blue-colored regions represent introgressions (defined by ≥5 SNPs) from temperate japonica into indica; variety names (on left) colored dark blue indicate indica accessions carrying a waxy allele introgressed from temperate japonica; those without waxy introgression indicated in red. (B) Admixture mapping p-values for amylose content using the temperate japonica component in the admixed subpopulation. (C) Association mapping p-values for amylose content in all accessions using mixed model approach. Horizontal dotted lines in both (B) and (C) represent significance values of 0.05 after Bonferroni correction.
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2875394&req=5

pone-0010780-g004: Regions of introgression from temperate japonica into indica aligned with admixture mapping and association mapping p-values for amylose content.Genome position of SNPs and introgressions indicated across the bottom; vertical grey lines indicate chromosomes; position of Waxy gene on chromosome 6 shown as vertical dashed line. (A) Horizontal grey lines indicate accessions; blue-colored regions represent introgressions (defined by ≥5 SNPs) from temperate japonica into indica; variety names (on left) colored dark blue indicate indica accessions carrying a waxy allele introgressed from temperate japonica; those without waxy introgression indicated in red. (B) Admixture mapping p-values for amylose content using the temperate japonica component in the admixed subpopulation. (C) Association mapping p-values for amylose content in all accessions using mixed model approach. Horizontal dotted lines in both (B) and (C) represent significance values of 0.05 after Bonferroni correction.
Mentions: The glutinous phenotype of rice is largely controlled by the Waxy (Wx) gene, located at 1.7 Mb on the short arm of chromosome 6. Waxy is a granule-bound starch synthase that is responsible for amylose biosynthesis in the grain [65]. There are two major functional haplotype groups of Wx that differentiate the Indica and Japonica rice varietal groups, with Wxa found mostly in Indica and Wxb mostly in Japonica. The amylose content is significantly lower in the Wxb haplotype [66]. In our study, the indica varieties Ming Hui, Sundensis, IR-44595, 93-11, Yang Dao 6, and Minghui 63 have a temperate japonica introgression at the Wx locus (Figure 4A). A SNP at the functional G/T mutation in intron 1 that is indicative of the Wxb haplotype [67] was included on our GoldenGate assay and our genotyping results confirmed that all of the indica varieties carrying the introgression marked by the T-allele have significantly lower amylose content (all less than 18.5% with mean = 14.1%) than those carrying the G-allele (all no less than 20% with mean = 23.6%).

Bottom Line: Our introgression analysis shows that most accessions exhibit some degree of admixture, with many individuals within a population sharing the same introgressed segment due to artificial selection.Admixture mapping and association analysis of amylose content and grain length illustrate the potential for dissecting the genetic basis of complex traits in domesticated plant populations.These analyses highlight the power of population genomics in agricultural systems to identify functionally important regions of the genome and to decipher the role of human-directed breeding in refashioning the genomes of a domesticated species.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Statistics and Computational Biology, Cornell University, Ithaca, New York, USA.

ABSTRACT

Background: The domestication of Asian rice (Oryza sativa) was a complex process punctuated by episodes of introgressive hybridization among and between subpopulations. Deep genetic divergence between the two main varietal groups (Indica and Japonica) suggests domestication from at least two distinct wild populations. However, genetic uniformity surrounding key domestication genes across divergent subpopulations suggests cultural exchange of genetic material among ancient farmers.

Methodology/principal findings: In this study, we utilize a novel 1,536 SNP panel genotyped across 395 diverse accessions of O. sativa to study genome-wide patterns of polymorphism, to characterize population structure, and to infer the introgression history of domesticated Asian rice. Our population structure analyses support the existence of five major subpopulations (indica, aus, tropical japonica, temperate japonica and GroupV) consistent with previous analyses. Our introgression analysis shows that most accessions exhibit some degree of admixture, with many individuals within a population sharing the same introgressed segment due to artificial selection. Admixture mapping and association analysis of amylose content and grain length illustrate the potential for dissecting the genetic basis of complex traits in domesticated plant populations.

Conclusions/significance: Genes in these regions control a myriad of traits including plant stature, blast resistance, and amylose content. These analyses highlight the power of population genomics in agricultural systems to identify functionally important regions of the genome and to decipher the role of human-directed breeding in refashioning the genomes of a domesticated species.

Show MeSH
Related in: MedlinePlus