Rapid evolutionary adaptation to heavy metal-polluted soils in plant species of the genus Arabidopsis

受到人为污染的有毒重金属污染的土壤的定植是植物快速进化适应过程的一个有前途的模型。在富含炉甘石族金属（锌（Zn）、镉（Cd）和铅（Pb））的土壤上建立种群的大量平行事件仅发生在拟南芥（A. thaliana）姐妹进化枝的物种中。 有趣的是，此类含金属地点的一小部分不仅拥有 Halleri，而且还拥有密切相关的物种 A. arenosa。在这些地点，两个物种中与中间金属相关的生理学以及一些具有中间形态的植物的出现表明了反复发生的种间杂交的可能性。在这里，我们的目的是探讨 A. Halleri 和 A. arenosa 之间的基因流在这两个物种适应炉甘石金属土壤中的作用，并与每个物种内的选择作用进行比较。 A. Halleri 对含金属土壤的适应仅仅需要进化出增强的金属超耐受性。由于 Zn 和 Cd 的超积累，即使在未受污染的土壤上，A. Halleri 也已表现出对炉甘石金属的全物种超耐受性，其浓度分别高达 >3,000 和 >100 µg g-1 干叶生物量。含金属土壤上的 A. Halleri 增强的金属超耐受性已被证明涉及金属超积累的减弱。相比之下，像几乎所有其他植物一样，沙仁通常是金属排除物种。我们在这里重点关注地理上聚集的炉甘石重金属污染和未污染地点组，其中 A. Halleri 和 A. arenosa 如今在田间自然生长。这些是通过与仅拥有两个物种之一的非金属参考地点相关的比较方法进行分析的。我们评估物种间基因渗入，并定位代表从其他物种渗入的单倍型的基因组区域。与此同时，我们应用基因组扫描方法来识别两个物种中任何一个物种中经过选择的基因组区域，这是第一阶段的延续，我们将这种方法应用于 A. Halleri 中罕见的铜过度耐受事件。为了测试适应的分子表型后果，我们比较了两个物种的选定群体中的基因表达。在这些地点收集的形态中间植物个体中，我们表征了田间的叶子和土壤组成，以获得初始表型信息。我们通过与两个假设的亲本物种进行比较来确定倍性水平，并在序列水平上分析源自 A. Halleri 和 A. arenosa 的基因组成分的植物。

The colonization of soils anthropogenically polluted with toxic levels of heavy metals is a promising model for processes of rapid evolutionary adaptation in plants. A large number of parallel incidences of the establishment of populations on soils enriched in the calamine group of metals – zinc (Zn), cadmium (Cd) and lead (Pb) – have occurred only in Arabidopsis halleri among the species in the sister clade of A. thaliana. Interestingly, a small subset of such metalliferous sites host not only A. halleri but also the closely related species A. arenosa. At these sites, the intermediate metal-related physiology in both species as well as the occurrence of a few plants of intermediate morphology suggest the possibility of recurrent inter-species hybridization. Here we aim to address the role of gene flow between A. halleri and A. arenosa in the adaptation of both species to calamine metalliferous soils, as compared to the role of selection within each species individually. The adaptation of A. halleri to metalliferous soils merely required the evolution of enhanced metal hypertolerance. A. halleri already exhibits species-wide hypertolerance to calamine metals as a result of the hyperaccumulation of Zn and Cd to extraordinarily high concentrations of >3,000 and >100 µg g-1 dry leaf biomass, respectively, even on non-contaminated soils. Enhanced metal hypertolerance in A. halleri on metalliferous soils has been shown to involve an attenuation of metal hyperaccumulation. By contrast, A. arenosa is generally a metal excluder species, like almost all other plants. We focus here on geographically clustered site groups of calamine heavy metal-contaminated and non-contaminated sites where both A. halleri and A. arenosa naturally grow together in the field today. These are analysed in a comparative approach in relation to non-metalliferous reference sites hosting only one of the two species. We assess between-species introgression genome-wide and localize genomic regions representing haplotypes introgressed from the other species. In parallel, we apply genome scan approaches to identify genomic regions that have been subject to selection in either of the two species, in continuation of the first phase where we applied this approach to the rare incidences of copper hypertolerance in A. halleri. To test for molecular phenotypic consequences of adaptation, we compare gene expression among a chosen set of populations of both species. In morphologically intermediate plant individuals collected at these sites, we characterize leaf and soil composition in the field to obtain initial phenotypic information. We determine ploidy levels by comparison to the two hypothesized parental species, and we analyse plants at the sequence level with respect to the genomic components originating from A. halleri and A. arenosa.