Rapid functional divergence after small-scale gene duplication in grasses

Abstract Background Gene duplication has played an important role in the evolution and domestication of flowering plants. Yet little is known about how plant duplicate genes evolve and are retained over long timescales, particularly those arising from small-scale duplication (SSD) rather than whole-...

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Main Authors: Xueyuan Jiang, Raquel Assis
Format: Article
Language:English
Published: BMC 2019-05-01
Series:BMC Evolutionary Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12862-019-1415-2
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spelling doaj-b7182bb7b4d242cb9e440afb4e9342252021-09-02T12:02:40ZengBMCBMC Evolutionary Biology1471-21482019-05-0119111110.1186/s12862-019-1415-2Rapid functional divergence after small-scale gene duplication in grassesXueyuan Jiang0Raquel Assis1Huck Institutes of the Life Sciences, Pennsylvania State UniversityHuck Institutes of the Life Sciences, Pennsylvania State UniversityAbstract Background Gene duplication has played an important role in the evolution and domestication of flowering plants. Yet little is known about how plant duplicate genes evolve and are retained over long timescales, particularly those arising from small-scale duplication (SSD) rather than whole-genome duplication (WGD) events. Results We address this question in the Poaceae (grass) family by analyzing gene expression data from nine tissues of Brachypodium distachyon, Oryza sativa japonica (rice), and Sorghum bicolor (sorghum). Consistent with theoretical predictions, expression profiles of most grass genes are conserved after SSD, suggesting that functional conservation is the primary outcome of SSD in grasses. However, we also uncover support for widespread functional divergence, much of which occurs asymmetrically via the process of neofunctionalization. Moreover, neofunctionalization preferentially targets younger (child) duplicate gene copies, is associated with RNA-mediated duplication, and occurs quickly after duplication. Further analysis reveals that functional divergence of SSD-derived genes is positively correlated with both sequence divergence and tissue specificity in all three grass species, and particularly with anther expression in B. distachyon. Conclusions Our results suggest that SSD-derived grass genes often undergo rapid functional divergence that may be driven by natural selection on male-specific phenotypes. These observations are consistent with those in several animal species, suggesting that duplicate genes take similar evolutionary trajectories in plants and animals.http://link.springer.com/article/10.1186/s12862-019-1415-2Gene duplicationExpression divergenceNeofunctionalization
collection DOAJ
language English
format Article
sources DOAJ
author Xueyuan Jiang
Raquel Assis
spellingShingle Xueyuan Jiang
Raquel Assis
Rapid functional divergence after small-scale gene duplication in grasses
BMC Evolutionary Biology
Gene duplication
Expression divergence
Neofunctionalization
author_facet Xueyuan Jiang
Raquel Assis
author_sort Xueyuan Jiang
title Rapid functional divergence after small-scale gene duplication in grasses
title_short Rapid functional divergence after small-scale gene duplication in grasses
title_full Rapid functional divergence after small-scale gene duplication in grasses
title_fullStr Rapid functional divergence after small-scale gene duplication in grasses
title_full_unstemmed Rapid functional divergence after small-scale gene duplication in grasses
title_sort rapid functional divergence after small-scale gene duplication in grasses
publisher BMC
series BMC Evolutionary Biology
issn 1471-2148
publishDate 2019-05-01
description Abstract Background Gene duplication has played an important role in the evolution and domestication of flowering plants. Yet little is known about how plant duplicate genes evolve and are retained over long timescales, particularly those arising from small-scale duplication (SSD) rather than whole-genome duplication (WGD) events. Results We address this question in the Poaceae (grass) family by analyzing gene expression data from nine tissues of Brachypodium distachyon, Oryza sativa japonica (rice), and Sorghum bicolor (sorghum). Consistent with theoretical predictions, expression profiles of most grass genes are conserved after SSD, suggesting that functional conservation is the primary outcome of SSD in grasses. However, we also uncover support for widespread functional divergence, much of which occurs asymmetrically via the process of neofunctionalization. Moreover, neofunctionalization preferentially targets younger (child) duplicate gene copies, is associated with RNA-mediated duplication, and occurs quickly after duplication. Further analysis reveals that functional divergence of SSD-derived genes is positively correlated with both sequence divergence and tissue specificity in all three grass species, and particularly with anther expression in B. distachyon. Conclusions Our results suggest that SSD-derived grass genes often undergo rapid functional divergence that may be driven by natural selection on male-specific phenotypes. These observations are consistent with those in several animal species, suggesting that duplicate genes take similar evolutionary trajectories in plants and animals.
topic Gene duplication
Expression divergence
Neofunctionalization
url http://link.springer.com/article/10.1186/s12862-019-1415-2
work_keys_str_mv AT xueyuanjiang rapidfunctionaldivergenceaftersmallscalegeneduplicationingrasses
AT raquelassis rapidfunctionaldivergenceaftersmallscalegeneduplicationingrasses
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