Natural selection in gene-dense regions shapes the genomic pattern of polymorphism in wild and domesticated rice

Jonathan M. Flowers, Jeanmaire Molina, Samara Rubinstein, Pu Huang, Barbara A. Schaal, Michael D. Purugganan

Research output: Contribution to journalArticle

Abstract

Levels of nucleotide variability are frequently positively correlated with recombination rate and negatively associated with gene density due to the effects of selection on linked variation. These relationships are determined by properties that frequently differ among species, including the mating system, and aspects of genome organization such as how genes are distributed along chromosomes. In rice, genes are found at highest density in regions with frequent crossing-over. This association between gene density and recombination rate provides an opportunity to evaluate the effects of selection in a genomic context that differs from other model organisms. Using single-nucleotide polymorphism data from Asian domesticated rice Oryza sativa ssp. japonica and ssp. indica and their progenitor species O. rufipogon, we observe a significant negative association between levels of polymorphism and both gene and coding site density, but either no association, or a negative correlation, between nucleotide variability and recombination rate. We establish that these patterns are unlikely to be explained by neutral mutation rate biases and demonstrate that a model of background selection with variable rates of deleterious mutation is sufficient to account for the gene density effect in O. rufipogon. In O. sativa ssp. japonica, we report a strong negative correlation between polymorphism and recombination rate and greater losses of variation during domestication in the euchromatic chromosome arms than heterochromatin. This is consistent with Hill-Robertson interference in low-recombination regions, which may limit the efficacy of selection for domestication traits. Our results suggest that the physical distribution of selected mutations is a primary factor that determines the genomic pattern of polymorphism in wild and domesticated rice species.

Original languageEnglish (US)
Pages (from-to)675-687
Number of pages13
JournalMolecular Biology and Evolution
Volume29
Issue number2
DOIs
StatePublished - Feb 2012

Fingerprint

Genetic Selection
natural selection
genomics
polymorphism
rice
Genetic Recombination
recombination
genetic polymorphism
gene
Genes
mutation
genes
domestication
Mutation Rate
chromosome
Oryza sativa
Nucleotides
Chromosomes
nucleotides
Oryza rufipogon

Keywords

  • background selection
  • deleterious mutation
  • domestication
  • Hill-Robertson
  • hitchhiking
  • interference
  • selfing

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Natural selection in gene-dense regions shapes the genomic pattern of polymorphism in wild and domesticated rice. / Flowers, Jonathan M.; Molina, Jeanmaire; Rubinstein, Samara; Huang, Pu; Schaal, Barbara A.; Purugganan, Michael D.

In: Molecular Biology and Evolution, Vol. 29, No. 2, 02.2012, p. 675-687.

Research output: Contribution to journalArticle

@article{75f481269b28486e9313ea2fdbdd37a7,
title = "Natural selection in gene-dense regions shapes the genomic pattern of polymorphism in wild and domesticated rice",
abstract = "Levels of nucleotide variability are frequently positively correlated with recombination rate and negatively associated with gene density due to the effects of selection on linked variation. These relationships are determined by properties that frequently differ among species, including the mating system, and aspects of genome organization such as how genes are distributed along chromosomes. In rice, genes are found at highest density in regions with frequent crossing-over. This association between gene density and recombination rate provides an opportunity to evaluate the effects of selection in a genomic context that differs from other model organisms. Using single-nucleotide polymorphism data from Asian domesticated rice Oryza sativa ssp. japonica and ssp. indica and their progenitor species O. rufipogon, we observe a significant negative association between levels of polymorphism and both gene and coding site density, but either no association, or a negative correlation, between nucleotide variability and recombination rate. We establish that these patterns are unlikely to be explained by neutral mutation rate biases and demonstrate that a model of background selection with variable rates of deleterious mutation is sufficient to account for the gene density effect in O. rufipogon. In O. sativa ssp. japonica, we report a strong negative correlation between polymorphism and recombination rate and greater losses of variation during domestication in the euchromatic chromosome arms than heterochromatin. This is consistent with Hill-Robertson interference in low-recombination regions, which may limit the efficacy of selection for domestication traits. Our results suggest that the physical distribution of selected mutations is a primary factor that determines the genomic pattern of polymorphism in wild and domesticated rice species.",
keywords = "background selection, deleterious mutation, domestication, Hill-Robertson, hitchhiking, interference, selfing",
author = "Flowers, {Jonathan M.} and Jeanmaire Molina and Samara Rubinstein and Pu Huang and Schaal, {Barbara A.} and Purugganan, {Michael D.}",
year = "2012",
month = "2",
doi = "10.1093/molbev/msr225",
language = "English (US)",
volume = "29",
pages = "675--687",
journal = "Molecular Biology and Evolution",
issn = "0737-4038",
publisher = "Oxford University Press",
number = "2",

}

TY - JOUR

T1 - Natural selection in gene-dense regions shapes the genomic pattern of polymorphism in wild and domesticated rice

AU - Flowers, Jonathan M.

AU - Molina, Jeanmaire

AU - Rubinstein, Samara

AU - Huang, Pu

AU - Schaal, Barbara A.

AU - Purugganan, Michael D.

PY - 2012/2

Y1 - 2012/2

N2 - Levels of nucleotide variability are frequently positively correlated with recombination rate and negatively associated with gene density due to the effects of selection on linked variation. These relationships are determined by properties that frequently differ among species, including the mating system, and aspects of genome organization such as how genes are distributed along chromosomes. In rice, genes are found at highest density in regions with frequent crossing-over. This association between gene density and recombination rate provides an opportunity to evaluate the effects of selection in a genomic context that differs from other model organisms. Using single-nucleotide polymorphism data from Asian domesticated rice Oryza sativa ssp. japonica and ssp. indica and their progenitor species O. rufipogon, we observe a significant negative association between levels of polymorphism and both gene and coding site density, but either no association, or a negative correlation, between nucleotide variability and recombination rate. We establish that these patterns are unlikely to be explained by neutral mutation rate biases and demonstrate that a model of background selection with variable rates of deleterious mutation is sufficient to account for the gene density effect in O. rufipogon. In O. sativa ssp. japonica, we report a strong negative correlation between polymorphism and recombination rate and greater losses of variation during domestication in the euchromatic chromosome arms than heterochromatin. This is consistent with Hill-Robertson interference in low-recombination regions, which may limit the efficacy of selection for domestication traits. Our results suggest that the physical distribution of selected mutations is a primary factor that determines the genomic pattern of polymorphism in wild and domesticated rice species.

AB - Levels of nucleotide variability are frequently positively correlated with recombination rate and negatively associated with gene density due to the effects of selection on linked variation. These relationships are determined by properties that frequently differ among species, including the mating system, and aspects of genome organization such as how genes are distributed along chromosomes. In rice, genes are found at highest density in regions with frequent crossing-over. This association between gene density and recombination rate provides an opportunity to evaluate the effects of selection in a genomic context that differs from other model organisms. Using single-nucleotide polymorphism data from Asian domesticated rice Oryza sativa ssp. japonica and ssp. indica and their progenitor species O. rufipogon, we observe a significant negative association between levels of polymorphism and both gene and coding site density, but either no association, or a negative correlation, between nucleotide variability and recombination rate. We establish that these patterns are unlikely to be explained by neutral mutation rate biases and demonstrate that a model of background selection with variable rates of deleterious mutation is sufficient to account for the gene density effect in O. rufipogon. In O. sativa ssp. japonica, we report a strong negative correlation between polymorphism and recombination rate and greater losses of variation during domestication in the euchromatic chromosome arms than heterochromatin. This is consistent with Hill-Robertson interference in low-recombination regions, which may limit the efficacy of selection for domestication traits. Our results suggest that the physical distribution of selected mutations is a primary factor that determines the genomic pattern of polymorphism in wild and domesticated rice species.

KW - background selection

KW - deleterious mutation

KW - domestication

KW - Hill-Robertson

KW - hitchhiking

KW - interference

KW - selfing

UR - http://www.scopus.com/inward/record.url?scp=84855455949&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84855455949&partnerID=8YFLogxK

U2 - 10.1093/molbev/msr225

DO - 10.1093/molbev/msr225

M3 - Article

C2 - 21917724

AN - SCOPUS:84855455949

VL - 29

SP - 675

EP - 687

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

SN - 0737-4038

IS - 2

ER -