Natural variation in stomata size contributes to the local adaptation of water-use efficiency in Arabidopsis thaliana

Stomata control gas exchanges between the plant and the atmosphere. How natural variation in stomata size and density contributes to resolve trade‐offs between carbon uptake and water‐loss in response to local climatic variation is not yet understood. We developed an automated confocal microscopy approach to characterize natural genetic variation in stomatal patterning in 330 fully‐sequenced Arabidopsis thaliana accessions collected throughout the European range of the species. We compared this to variation in water‐use efficiency, measured as carbon isotope discrimination (δ13C). We detect substantial genetic variation for stomata size and density segregating within Arabidopsis thaliana. A positive correlation between stomata size and δ13C further suggests that this variation has consequences on water‐use efficiency. Genome‐wide association analyses indicate a complex genetic architecture underlying not only variation in stomata patterning but also to its co‐variation with carbon uptake parameters. Yet, we report two novel QTL affecting δ13C independently of stomata patterning. This suggests that, in A. thaliana, both morphological and physiological variants contribute to genetic variance in water‐use efficiency. Patterns of regional differentiation and co‐variation with climatic parameters indicate that natural selection has contributed to shape some of this variation, especially in Southern Sweden, where water availability is more limited in spring relative to summer. These conditions are expected to favor the evolution of drought avoidance mechanisms over drought escape strategies.

气孔（stomata）介导植物与大气间的气体交换。目前学界尚未明确，气孔大小与密度的自然变异如何帮助植物响应局地气候变异，协调碳摄取与水分流失间的权衡关系。本研究开发了自动化共聚焦显微镜方法，对覆盖该物种欧洲分布范围的330份全基因组测序的拟南芥（Arabidopsis thaliana）种质资源的气孔格局自然遗传变异进行表征，并将该结果与以碳同位素判别值（δ¹³C）衡量的水分利用效率变异进行对比。本研究检测到拟南芥群体内气孔大小与密度存在丰富的分离遗传变异。气孔大小与δ¹³C呈正相关，进一步表明该变异会对水分利用效率产生影响。全基因组关联分析显示，不仅气孔格局变异存在复杂的遗传基础，其与碳摄取参数的协同变异亦是如此。然而，本研究报道了两个独立于气孔格局、可影响δ¹³C的全新数量性状基因座（QTL）。这表明在拟南芥中，形态学与生理学变异均会对水分利用效率的遗传方差产生贡献。区域分化模式以及与气候参数的协同变异表明，自然选择参与塑造了部分此类变异，尤其在瑞典南部地区——该区域春季的水分可利用性相较于夏季更为匮乏。此类环境条件更倾向于促进耐旱机制的演化，而非避旱策略。