The Phenotypic Plasticity of Duplicated Genes in Saccharomyces cerevisiae and the Origin of Adaptations

Gene and genome duplication are the major sources of biological innovations in plants and animals. Functional and transcriptional divergence between the copies after gene duplication has been considered the main driver of innovations . However, here we show that increased phenotypic plasticity after...

Full description

Bibliographic Details
Main Authors: Florian Mattenberger, Beatriz Sabater-Muñoz, Christina Toft, Mario A. Fares
Format: Article
Language:English
Published: Oxford University Press 2017-01-01
Series:G3: Genes, Genomes, Genetics
Subjects:
Online Access:http://g3journal.org/lookup/doi/10.1534/g3.116.035329
id doaj-2da9a40c0fa04686b614a9e5064c92de
record_format Article
spelling doaj-2da9a40c0fa04686b614a9e5064c92de2021-07-02T08:37:41ZengOxford University PressG3: Genes, Genomes, Genetics2160-18362017-01-0171637510.1534/g3.116.0353296The Phenotypic Plasticity of Duplicated Genes in Saccharomyces cerevisiae and the Origin of AdaptationsFlorian MattenbergerBeatriz Sabater-MuñozChristina ToftMario A. FaresGene and genome duplication are the major sources of biological innovations in plants and animals. Functional and transcriptional divergence between the copies after gene duplication has been considered the main driver of innovations . However, here we show that increased phenotypic plasticity after duplication plays a more major role than thought before in the origin of adaptations. We perform an exhaustive analysis of the transcriptional alterations of duplicated genes in the unicellular eukaryote Saccharomyces cerevisiae when challenged with five different environmental stresses. Analysis of the transcriptomes of yeast shows that gene duplication increases the transcriptional response to environmental changes, with duplicated genes exhibiting signatures of adaptive transcriptional patterns in response to stress. The mechanism of duplication matters, with whole-genome duplicates being more transcriptionally altered than small-scale duplicates. The predominant transcriptional pattern follows the classic theory of evolution by gene duplication; with one gene copy remaining unaltered under stress, while its sister copy presents large transcriptional plasticity and a prominent role in adaptation. Moreover, we find additional transcriptional profiles that are suggestive of neo- and subfunctionalization of duplicate gene copies. These patterns are strongly correlated with the functional dependencies and sequence divergence profiles of gene copies. We show that, unlike singletons, duplicates respond more specifically to stress, supporting the role of natural selection in the transcriptional plasticity of duplicates. Our results reveal the underlying transcriptional complexity of duplicated genes and its role in the origin of adaptations.http://g3journal.org/lookup/doi/10.1534/g3.116.035329evolutionary biologygene functionsmall-scale duplicateswhole-genome duplicatestranscriptional profiles
collection DOAJ
language English
format Article
sources DOAJ
author Florian Mattenberger
Beatriz Sabater-Muñoz
Christina Toft
Mario A. Fares
spellingShingle Florian Mattenberger
Beatriz Sabater-Muñoz
Christina Toft
Mario A. Fares
The Phenotypic Plasticity of Duplicated Genes in Saccharomyces cerevisiae and the Origin of Adaptations
G3: Genes, Genomes, Genetics
evolutionary biology
gene function
small-scale duplicates
whole-genome duplicates
transcriptional profiles
author_facet Florian Mattenberger
Beatriz Sabater-Muñoz
Christina Toft
Mario A. Fares
author_sort Florian Mattenberger
title The Phenotypic Plasticity of Duplicated Genes in Saccharomyces cerevisiae and the Origin of Adaptations
title_short The Phenotypic Plasticity of Duplicated Genes in Saccharomyces cerevisiae and the Origin of Adaptations
title_full The Phenotypic Plasticity of Duplicated Genes in Saccharomyces cerevisiae and the Origin of Adaptations
title_fullStr The Phenotypic Plasticity of Duplicated Genes in Saccharomyces cerevisiae and the Origin of Adaptations
title_full_unstemmed The Phenotypic Plasticity of Duplicated Genes in Saccharomyces cerevisiae and the Origin of Adaptations
title_sort phenotypic plasticity of duplicated genes in saccharomyces cerevisiae and the origin of adaptations
publisher Oxford University Press
series G3: Genes, Genomes, Genetics
issn 2160-1836
publishDate 2017-01-01
description Gene and genome duplication are the major sources of biological innovations in plants and animals. Functional and transcriptional divergence between the copies after gene duplication has been considered the main driver of innovations . However, here we show that increased phenotypic plasticity after duplication plays a more major role than thought before in the origin of adaptations. We perform an exhaustive analysis of the transcriptional alterations of duplicated genes in the unicellular eukaryote Saccharomyces cerevisiae when challenged with five different environmental stresses. Analysis of the transcriptomes of yeast shows that gene duplication increases the transcriptional response to environmental changes, with duplicated genes exhibiting signatures of adaptive transcriptional patterns in response to stress. The mechanism of duplication matters, with whole-genome duplicates being more transcriptionally altered than small-scale duplicates. The predominant transcriptional pattern follows the classic theory of evolution by gene duplication; with one gene copy remaining unaltered under stress, while its sister copy presents large transcriptional plasticity and a prominent role in adaptation. Moreover, we find additional transcriptional profiles that are suggestive of neo- and subfunctionalization of duplicate gene copies. These patterns are strongly correlated with the functional dependencies and sequence divergence profiles of gene copies. We show that, unlike singletons, duplicates respond more specifically to stress, supporting the role of natural selection in the transcriptional plasticity of duplicates. Our results reveal the underlying transcriptional complexity of duplicated genes and its role in the origin of adaptations.
topic evolutionary biology
gene function
small-scale duplicates
whole-genome duplicates
transcriptional profiles
url http://g3journal.org/lookup/doi/10.1534/g3.116.035329
work_keys_str_mv AT florianmattenberger thephenotypicplasticityofduplicatedgenesinsaccharomycescerevisiaeandtheoriginofadaptations
AT beatrizsabatermunoz thephenotypicplasticityofduplicatedgenesinsaccharomycescerevisiaeandtheoriginofadaptations
AT christinatoft thephenotypicplasticityofduplicatedgenesinsaccharomycescerevisiaeandtheoriginofadaptations
AT marioafares thephenotypicplasticityofduplicatedgenesinsaccharomycescerevisiaeandtheoriginofadaptations
AT florianmattenberger phenotypicplasticityofduplicatedgenesinsaccharomycescerevisiaeandtheoriginofadaptations
AT beatrizsabatermunoz phenotypicplasticityofduplicatedgenesinsaccharomycescerevisiaeandtheoriginofadaptations
AT christinatoft phenotypicplasticityofduplicatedgenesinsaccharomycescerevisiaeandtheoriginofadaptations
AT marioafares phenotypicplasticityofduplicatedgenesinsaccharomycescerevisiaeandtheoriginofadaptations
_version_ 1721334480404217856