Adaptation to warmer climates by parallel functional evolution of CBF genes in Arabidopsis thaliana

J. Grey Monroe, Cullen McGovern, Jesse R. Lasky, Kelsi Grogan, James Beck, John K. McKay

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

The evolutionary processes and genetics underlying local adaptation at a specieswide level are largely unknown. Recent work has indicated that a frameshift mutation in a member of a family of transcription factors, C-repeat binding factors or CBFs, underlies local adaptation and freezing tolerance divergence between two European populations of Arabidopsis thaliana. To ask whether the specieswide evolution of CBF genes in Arabidopsis is consistent with local adaptation, we surveyed CBF variation from 477 wild accessions collected across the species' range. We found that CBF sequence variation is strongly associated with winter temperature variables. Looking specifically at the minimum temperature experienced during the coldest month, we found that Arabidopsis from warmer climates exhibit a significant excess of nonsynonymous polymorphisms in CBF genes and revealed a CBF haplotype network whose structure points to multiple independent transitions to warmer climates. We also identified a number of newly described mutations of significant functional effect in CBF genes, similar to the frameshift mutation previously indicated to be locally adaptive in Italy, and find that they are significantly associated with warm winters. Lastly, we uncover relationships between climate and the position of significant functional effect mutations between and within CBF paralogs, suggesting variation in adaptive function of different mutations. Cumulatively, these findings support the hypothesis that disruption of CBF gene function is adaptive in warmer climates, and illustrate how parallel evolution in a transcription factor can underlie adaptation to climate.

Original languageEnglish (US)
Pages (from-to)3632-3644
Number of pages13
JournalMolecular ecology
Volume25
Issue number15
DOIs
StatePublished - Aug 1 2016

Fingerprint

Climate
Arabidopsis
mutation
Arabidopsis thaliana
local adaptation
climate
gene
frameshift mutation
Frameshift Mutation
Genes
genes
Mutation
Transcription Factors
transcription factors
Genetic Phenomena
parallel evolution
Temperature
winter
gene targeting
cold tolerance

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

Monroe, J. Grey ; McGovern, Cullen ; Lasky, Jesse R. ; Grogan, Kelsi ; Beck, James ; McKay, John K. / Adaptation to warmer climates by parallel functional evolution of CBF genes in Arabidopsis thaliana. In: Molecular ecology. 2016 ; Vol. 25, No. 15. pp. 3632-3644.
@article{ed6f964e4f6a4a809817705f0efdd4cc,
title = "Adaptation to warmer climates by parallel functional evolution of CBF genes in Arabidopsis thaliana",
abstract = "The evolutionary processes and genetics underlying local adaptation at a specieswide level are largely unknown. Recent work has indicated that a frameshift mutation in a member of a family of transcription factors, C-repeat binding factors or CBFs, underlies local adaptation and freezing tolerance divergence between two European populations of Arabidopsis thaliana. To ask whether the specieswide evolution of CBF genes in Arabidopsis is consistent with local adaptation, we surveyed CBF variation from 477 wild accessions collected across the species' range. We found that CBF sequence variation is strongly associated with winter temperature variables. Looking specifically at the minimum temperature experienced during the coldest month, we found that Arabidopsis from warmer climates exhibit a significant excess of nonsynonymous polymorphisms in CBF genes and revealed a CBF haplotype network whose structure points to multiple independent transitions to warmer climates. We also identified a number of newly described mutations of significant functional effect in CBF genes, similar to the frameshift mutation previously indicated to be locally adaptive in Italy, and find that they are significantly associated with warm winters. Lastly, we uncover relationships between climate and the position of significant functional effect mutations between and within CBF paralogs, suggesting variation in adaptive function of different mutations. Cumulatively, these findings support the hypothesis that disruption of CBF gene function is adaptive in warmer climates, and illustrate how parallel evolution in a transcription factor can underlie adaptation to climate.",
author = "Monroe, {J. Grey} and Cullen McGovern and Lasky, {Jesse R.} and Kelsi Grogan and James Beck and McKay, {John K.}",
year = "2016",
month = "8",
day = "1",
doi = "10.1111/mec.13711",
language = "English (US)",
volume = "25",
pages = "3632--3644",
journal = "Molecular Ecology",
issn = "0962-1083",
publisher = "Wiley-Blackwell",
number = "15",

}

Adaptation to warmer climates by parallel functional evolution of CBF genes in Arabidopsis thaliana. / Monroe, J. Grey; McGovern, Cullen; Lasky, Jesse R.; Grogan, Kelsi; Beck, James; McKay, John K.

In: Molecular ecology, Vol. 25, No. 15, 01.08.2016, p. 3632-3644.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Adaptation to warmer climates by parallel functional evolution of CBF genes in Arabidopsis thaliana

AU - Monroe, J. Grey

AU - McGovern, Cullen

AU - Lasky, Jesse R.

AU - Grogan, Kelsi

AU - Beck, James

AU - McKay, John K.

PY - 2016/8/1

Y1 - 2016/8/1

N2 - The evolutionary processes and genetics underlying local adaptation at a specieswide level are largely unknown. Recent work has indicated that a frameshift mutation in a member of a family of transcription factors, C-repeat binding factors or CBFs, underlies local adaptation and freezing tolerance divergence between two European populations of Arabidopsis thaliana. To ask whether the specieswide evolution of CBF genes in Arabidopsis is consistent with local adaptation, we surveyed CBF variation from 477 wild accessions collected across the species' range. We found that CBF sequence variation is strongly associated with winter temperature variables. Looking specifically at the minimum temperature experienced during the coldest month, we found that Arabidopsis from warmer climates exhibit a significant excess of nonsynonymous polymorphisms in CBF genes and revealed a CBF haplotype network whose structure points to multiple independent transitions to warmer climates. We also identified a number of newly described mutations of significant functional effect in CBF genes, similar to the frameshift mutation previously indicated to be locally adaptive in Italy, and find that they are significantly associated with warm winters. Lastly, we uncover relationships between climate and the position of significant functional effect mutations between and within CBF paralogs, suggesting variation in adaptive function of different mutations. Cumulatively, these findings support the hypothesis that disruption of CBF gene function is adaptive in warmer climates, and illustrate how parallel evolution in a transcription factor can underlie adaptation to climate.

AB - The evolutionary processes and genetics underlying local adaptation at a specieswide level are largely unknown. Recent work has indicated that a frameshift mutation in a member of a family of transcription factors, C-repeat binding factors or CBFs, underlies local adaptation and freezing tolerance divergence between two European populations of Arabidopsis thaliana. To ask whether the specieswide evolution of CBF genes in Arabidopsis is consistent with local adaptation, we surveyed CBF variation from 477 wild accessions collected across the species' range. We found that CBF sequence variation is strongly associated with winter temperature variables. Looking specifically at the minimum temperature experienced during the coldest month, we found that Arabidopsis from warmer climates exhibit a significant excess of nonsynonymous polymorphisms in CBF genes and revealed a CBF haplotype network whose structure points to multiple independent transitions to warmer climates. We also identified a number of newly described mutations of significant functional effect in CBF genes, similar to the frameshift mutation previously indicated to be locally adaptive in Italy, and find that they are significantly associated with warm winters. Lastly, we uncover relationships between climate and the position of significant functional effect mutations between and within CBF paralogs, suggesting variation in adaptive function of different mutations. Cumulatively, these findings support the hypothesis that disruption of CBF gene function is adaptive in warmer climates, and illustrate how parallel evolution in a transcription factor can underlie adaptation to climate.

UR - http://www.scopus.com/inward/record.url?scp=85027949377&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85027949377&partnerID=8YFLogxK

U2 - 10.1111/mec.13711

DO - 10.1111/mec.13711

M3 - Article

C2 - 27247130

AN - SCOPUS:85027949377

VL - 25

SP - 3632

EP - 3644

JO - Molecular Ecology

JF - Molecular Ecology

SN - 0962-1083

IS - 15

ER -