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 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.在物种全域范围内，局域适应背后的演化过程与遗传机制仍鲜为人知。已有研究表明，转录因子（transcription factors）家族成员之一的C-repeat结合因子（C-repeat binding factors, CBFs）中的一处移码突变（frameshift mutation），是欧洲两种拟南芥（Arabidopsis thaliana）种群间局域适应与耐寒性分化的遗传基础。为探究拟南芥CBF基因的物种尺度演化是否符合局域适应理论，本研究对覆盖该物种自然分布范围的477份野生种质资源的CBF基因变异开展了系统性检测与分析。研究发现，CBF基因的序列变异与冬季温度变量显著相关。针对最冷月最低温度这一指标展开专项分析后，我们发现来自温暖气候区域的拟南芥，其CBF基因中存在显著过量的非同义多态性（nonsynonymous polymorphisms）；同时解析得到一个CBF单倍型网络（haplotype network），其结构特征暗示存在多次独立向温暖气候环境的适应性演化转变。此外，我们在CBF基因中鉴定出多个此前未被报道的、具有显著功能效应的突变位点——这类突变与此前在意大利被发现的局域适应性移码突变特征相似，且这些突变与暖冬气候显著相关。最后，我们揭示了气候与CBF旁系同源基因（paralogs）之间及内部的功能效应突变位点分布间的关联，这提示不同突变的适应性功能存在差异。综合来看，上述研究结果支持"CBF基因功能丧失在温暖气候环境中具有适应性优势"这一假说，并阐明了转录因子的平行演化如何为气候适应提供遗传基础。