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

The evolutionary processes and genetics underlying local adaptation at a species wide 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 species-wide 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 non-synonymous 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.

在物种全局尺度下，支撑局部适应的进化过程与遗传机制仍未得到充分阐明。近期研究证实，转录因子家族成员C-重复结合因子（C-repeat binding factors, CBFs）的一处移码突变，是欧洲两个拟南芥（Arabidopsis thaliana）种群间局部适应与冻耐受分化的关键遗传基础。为验证拟南芥CBF基因的物种尺度进化是否契合局部适应假说，我们对覆盖该物种全球分布范围的477份野生种质材料的CBF基因变异情况开展了调查分析。研究结果显示，CBF基因的序列变异与冬季温度变量存在显著相关性。针对最冷月最低温这一指标进行专项分析后，我们发现：来自温暖气候区域的拟南芥种群，其CBF基因中存在显著过量的非同义多态性；同时解析得到的CBF单倍型网络结构表明，存在多起独立向温暖气候环境的适应性演化事件。我们还鉴定出一批新发现的、具有显著功能效应的CBF基因突变位点，其特征与此前报道的意大利当地适应性移码突变高度相似，且这些突变位点与暖冬气候存在显著关联。此外，我们还揭示了气候与CBF旁系同源基因间及内部的功能效应突变位点位置之间的关联，提示不同突变的适应性功能存在分化差异。综合以上研究结果，我们支持“CBF基因功能的失活在温暖气候环境中具备适应性优势”这一假说，并阐明了转录因子的平行演化如何作为气候适应的遗传基础。