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.
authors.affiliation: Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, 80523, USA.|Graduate Degree Program in Ecology, Colorado State University, Fort Collins, CO, 80523, USA.
authors.forename: J Grey
authors.initials: JG
authors.lastname: Monroe
authors.affiliation: Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, 80523, USA.
authors.forename: Cullen
authors.initials: C
authors.lastname: McGovern
authors.affiliation: Department of Biology, Pennsylvania State University, University Park, PA, 16802, USA.
authors.forename: Jesse R
authors.initials: JR
authors.lastname: Lasky
authors.affiliation: Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, 80523, USA.
authors.forename: Kelsi
authors.initials: K
authors.lastname: Grogan
authors.affiliation: Department of Biological Sciences, Wichita State University, Wichita, KS, 67260, USA.|Botanical Research Institute of Texas, Fort Worth, TX, 76107, USA.
authors.forename: James
authors.initials: J
authors.lastname: Beck
authors.affiliation: Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, 80523, USA.|Graduate Degree Program in Ecology, Colorado State University, Fort Collins, CO, 80523, USA.
authors.forename: John K
authors.initials: JK
authors.lastname: McKay
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics*; D017360:Arabidopsis / Q000235:genetics*; D029681:Arabidopsis Proteins / Q000235:genetics; D002980:Climate; D018506:Gene Expression Regulation, Plant; D005828:Genetics, Population; D007558:Italy; D013696:Temperature; D014157:Transcription Factors / Q000235:genetics
chemical_list: D029681:Arabidopsis Proteins; D014157:Transcription Factors
keywords: C-repeat binding factor; adaptation; climate; gene structure and function; landscape genetics; molecular evolution