Low Additive Genetic Variation in a Trait Under Selection in Domesticated Rice

Quantitative traits are important targets of both natural and artificial selection. The genetic architecture of these traits and its change during the adaptive process is thus of fundamental interest. The fate of the additive effects of variants underlying a trait receives particular attention becau...

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Main Authors: Nicholas G. Karavolias, Anthony J. Greenberg, Luz S. Barrero, Lyza G. Maron, Yuxin Shi, Eliana Monteverde, Miguel A. Piñeros, Susan R. McCouch
Format: Article
Language:English
Published: Oxford University Press 2020-07-01
Series:G3: Genes, Genomes, Genetics
Subjects:
Online Access:http://g3journal.org/lookup/doi/10.1534/g3.120.401194
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author Nicholas G. Karavolias
Anthony J. Greenberg
Luz S. Barrero
Lyza G. Maron
Yuxin Shi
Eliana Monteverde
Miguel A. Piñeros
Susan R. McCouch
author_facet Nicholas G. Karavolias
Anthony J. Greenberg
Luz S. Barrero
Lyza G. Maron
Yuxin Shi
Eliana Monteverde
Miguel A. Piñeros
Susan R. McCouch
author_sort Nicholas G. Karavolias
collection DOAJ
description Quantitative traits are important targets of both natural and artificial selection. The genetic architecture of these traits and its change during the adaptive process is thus of fundamental interest. The fate of the additive effects of variants underlying a trait receives particular attention because they constitute the genetic variation component that is transferred from parents to offspring and thus governs the response to selection. While estimation of this component of phenotypic variation is challenging, the increasing availability of dense molecular markers puts it within reach. Inbred plant species offer an additional advantage because phenotypes of genetically identical individuals can be measured in replicate. This makes it possible to estimate marker effects separately from the contribution of the genetic background not captured by genotyped loci. We focused on root growth in domesticated rice, Oryza sativa, under normal and aluminum (Al) stress conditions, a trait under recent selection because it correlates with survival under drought. A dense single nucleotide polymorphism (SNP) map is available for all accessions studied. Taking advantage of this map and a set of Bayesian models, we assessed additive marker effects. While total genetic variation accounted for a large proportion of phenotypic variance, marker effects contributed little information, particularly in the Al-tolerant tropical japonica population of rice. We were unable to identify any loci associated with root growth in this population. Models estimating the aggregate effects of all measured genotypes likewise produced low estimates of marker heritability and were unable to predict total genetic values accurately. Our results support the long-standing conjecture that additive genetic variation is depleted in traits under selection. We further provide evidence that this depletion is due to the prevalence of low-frequency alleles that underlie the trait.
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spelling doaj.art-e2a270e2d8944d938a52e68016e1de702022-12-21T22:52:09ZengOxford University PressG3: Genes, Genomes, Genetics2160-18362020-07-011072435244310.1534/g3.120.40119427Low Additive Genetic Variation in a Trait Under Selection in Domesticated RiceNicholas G. KaravoliasAnthony J. GreenbergLuz S. BarreroLyza G. MaronYuxin ShiEliana MonteverdeMiguel A. PiñerosSusan R. McCouchQuantitative traits are important targets of both natural and artificial selection. The genetic architecture of these traits and its change during the adaptive process is thus of fundamental interest. The fate of the additive effects of variants underlying a trait receives particular attention because they constitute the genetic variation component that is transferred from parents to offspring and thus governs the response to selection. While estimation of this component of phenotypic variation is challenging, the increasing availability of dense molecular markers puts it within reach. Inbred plant species offer an additional advantage because phenotypes of genetically identical individuals can be measured in replicate. This makes it possible to estimate marker effects separately from the contribution of the genetic background not captured by genotyped loci. We focused on root growth in domesticated rice, Oryza sativa, under normal and aluminum (Al) stress conditions, a trait under recent selection because it correlates with survival under drought. A dense single nucleotide polymorphism (SNP) map is available for all accessions studied. Taking advantage of this map and a set of Bayesian models, we assessed additive marker effects. While total genetic variation accounted for a large proportion of phenotypic variance, marker effects contributed little information, particularly in the Al-tolerant tropical japonica population of rice. We were unable to identify any loci associated with root growth in this population. Models estimating the aggregate effects of all measured genotypes likewise produced low estimates of marker heritability and were unable to predict total genetic values accurately. Our results support the long-standing conjecture that additive genetic variation is depleted in traits under selection. We further provide evidence that this depletion is due to the prevalence of low-frequency alleles that underlie the trait.http://g3journal.org/lookup/doi/10.1534/g3.120.401194heritability gwas abiotic stress stress tolerance
spellingShingle Nicholas G. Karavolias
Anthony J. Greenberg
Luz S. Barrero
Lyza G. Maron
Yuxin Shi
Eliana Monteverde
Miguel A. Piñeros
Susan R. McCouch
Low Additive Genetic Variation in a Trait Under Selection in Domesticated Rice
G3: Genes, Genomes, Genetics
heritability gwas abiotic stress stress tolerance
title Low Additive Genetic Variation in a Trait Under Selection in Domesticated Rice
title_full Low Additive Genetic Variation in a Trait Under Selection in Domesticated Rice
title_fullStr Low Additive Genetic Variation in a Trait Under Selection in Domesticated Rice
title_full_unstemmed Low Additive Genetic Variation in a Trait Under Selection in Domesticated Rice
title_short Low Additive Genetic Variation in a Trait Under Selection in Domesticated Rice
title_sort low additive genetic variation in a trait under selection in domesticated rice
topic heritability gwas abiotic stress stress tolerance
url http://g3journal.org/lookup/doi/10.1534/g3.120.401194
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