Genome-Wide Patterns of Nucleotide Polymorphism in Domesticated Rice

Department of Genetics, North Carolina State University, Raleigh, North Carolina, USA.
PLoS Genetics (Impact Factor: 7.53). 10/2007; 3(9):1745-56. DOI: 10.1371/journal.pgen.0030163
Source: PubMed


Domesticated Asian rice (Oryza sativa) is one of the oldest domesticated crop species in the world, having fed more people than any other plant in human history. We report the patterns of DNA sequence variation in rice and its wild ancestor, O. rufipogon, across 111 randomly chosen gene fragments, and use these to infer the evolutionary dynamics that led to the origins of rice. There is a genome-wide excess of high-frequency derived single nucleotide polymorphisms (SNPs) in O. sativa varieties, a pattern that has not been reported for other crop species. We developed several alternative models to explain contemporary patterns of polymorphisms in rice, including a (i) selectively neutral population bottleneck model, (ii) bottleneck plus migration model, (iii) multiple selective sweeps model, and (iv) bottleneck plus selective sweeps model. We find that a simple bottleneck model, which has been the dominant demographic model for domesticated species, cannot explain the derived nucleotide polymorphism site frequency spectrum in rice. Instead, a bottleneck model that incorporates selective sweeps, or a more complex demographic model that includes subdivision and gene flow, are more plausible explanations for patterns of variation in domesticated rice varieties. If selective sweeps are indeed the explanation for the observed nucleotide data of domesticated rice, it suggests that strong selection can leave its imprint on genome-wide polymorphism patterns, contrary to expectations that selection results only in a local signature of variation.

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Available from: Kenneth M Olsen, Oct 04, 2015
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    • "domesticated around 8200 to 13,000 years ago although the precise date of the first domestication is still unknown (Caicedo et al. 2007; Molina et al. 2011). The differences are due to estimates of the haploid effective population size N e for various species. "
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    ABSTRACT: The resistance gene Pi-ta has been effectively used to control rice blast disease, but some populations of cultivated and wild rice have evolved resistance. Insights into the evolutionary processes that led to this resistance during crop domestication may be inferred from the population history of domesticated and wild rice strains. In this study, we applied a recently developed statistical method, time-dependent Poisson random field model, to examine the evolution of the Pi-ta gene in cultivated and weedy rice. Our study suggests that the Pi-ta gene may have more recently introgressed into cultivated rice, indica and japonica, and U.S. weedy rice from the wild species, Oryza rufipogon. In addition, the Pi-ta gene is under positive selection in japonica, tropical japonica, U.S. cultivars and U.S. weedy rice. We also found that sequences of two domains of the Pi-ta gene, the nucleotide binding site (NBS) and leucine-rich repeat (LRR) domain, are highly conserved among all rice accessions examined. Our results provide a valuable analytical tool for understanding the evolution of disease resistance genes in crop plants.
    G3-Genes Genomes Genetics 10/2014; 4(12):2425-2432. DOI:10.1534/g3.114.014969 · 3.20 Impact Factor
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    • "For the generation of these four subpopulations, a burn-in length of 50,000 and run length of 100,000 iterations seemed to be sufficient for giving reasonably consistent values of maximum log likelihood across ten replicates. This observation was comparable to that documented earlier based on population structure analysis using microsatellite and SNP markers (Ni et al. 2002; Garris et al. 2003, 2005; Caicedo et al. 2007; Agrama et al. 2007). The level of diversity was comparable to that reported previously (Garris et al. 2005; Agrama et al. 2007) with microsatellite and SNP markers, but lower than (0.047–0.760 with an average of 0.470) that estimated with the microsatellite markers using a larger set of rice genotypes (Jin et al. 2010). "
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    ABSTRACT: Development and large-scale genotyping of single-nucleotide polymorphism (SNP) is required to use identified sequence variation in the alleles of different genes to determine their functional relevance to the candidate gene(s). In the present study, Illumina GoldenGate assay was used to validate and genotype SNPs in a set of six major rice blast resistance genes, viz. Pi-ta, Piz(t), Pi54, Pi9, Pi5(1) and Pib, distributed over five chromosomes, to understand their functional relevance and study the population structure in rice. All the selected SNPs loci (96) of six blast (Magna-porthe oryzae) resistance genes were genotyped successfully in 92 rice lines with an overall genotype call rate of 92.0 % and minimum GenTrain cutoff score of C0.448. The highest genotyped SNPs were found in japonica type (97.1 %) rice lines, followed by indica (92.12 %), indica basmati (91.84 %) and minimum in case of wild species (82.0 %). Among the genotyped loci, the highest score (98.68 %) was observed in case of Piz(t), followed by Pi-ta, Pi5(1), Pib, Pi54 and Pi9. Polymorphism was obtained in 87.5 % SNPs loci producing 7,728 genotype calls. Minor allele frequency ranged from 0.01 to 0.49 and Electronic supplementary material The online version of this article (doi:10.1007/s11032-014-0129-9) contains supple-mentary material, which is available to authorized users.
    Molecular Breeding 06/2014; 34(3). DOI:10.1007/s11032-014-0129-9 · 2.25 Impact Factor
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    • "This represents, on average, one SNP every 500 bp in the wild population and only one SNP every 1.6 kb in the protein-coding genes of O. glaberrima. Compared with other wild Oryza species, O. barthii is nearly four times less genetically diverse than O. rufipogon (p s = 0.0052, Caicedo et al. 2007). More generally, a p s value of 0.14% range among the lowest value in eukaryotes (Leffler et al. 2012). "
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    ABSTRACT: The African cultivated rice (Oryza glaberrima) was domesticated in West Africa 3,000 years ago. Although less cultivated than the Asian rice (O. sativa), O. glaberrima landraces often display interesting adaptation to rustic environment (e.g., drought). Here, using RNA-seq technology we were able to compare more than 12,000 transcripts between 9 O. glaberrima, 10 wild O. barthii and one O. meridionalis individuals. With a synonymous nucleotide diversity πs = 0.0006 per site, O. glaberrima appears as the least genetically diverse crop grass ever documented. Using Approximate Bayesian Computation, we estimated that O. glaberrima experienced a severe bottleneck during domestication. This demographic scenario almost fully accounts for the pattern of genetic diversity across O. glaberrima genome as we detected very few outliers regions where positive selection may have further impacted genetic diversity. Moreover, the large excess of derived non-synonymous substitution that we detected suggests that the O. glaberrima population suffered from the “cost of domestication”. In addition, we used this genome-scale dataset to demonstrate that (i) O. barthii genetic diversity is positively correlated with recombination rate and negatively with gene density; (ii) expression level is negatively correlated with evolutionary constraint and (iii) one region on chromosome 5 (position 4-6 Mb) exhibits a clear signature of introgression with a yet unidentified Oryza species. This work represents the first genome-wide survey of the African rice genetic diversity and paves the way for further comparison between the African and the Asian rice, notably regarding the genetics underlying domestication traits.This article is protected by copyright. All rights reserved.
    Molecular Ecology 03/2014; 23(9). DOI:10.1111/mec.12738 · 6.49 Impact Factor
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