Metal hyperaccumulation in plants is an ecological trait whose biological significance remains debated, in particular because the selective pressures that govern its evolutionary dynamics are complex. One of the possible causes of quantitative variation in hyperaccumulation may be local adaptation to metalliferous soils. Here, we explored the population genetic structure of Arabidopsis halleri at fourteen metalliferous and nonmetalliferous sampling sites in southern Poland. The results were integrated with a quantitative assessment of variation in zinc hyperaccumulation to trace local adaptation. We identified a clear hierarchical structure with two distinct genetic groups at the upper level of clustering. Interestingly, these groups corresponded to different geographic subregions, rather than to ecological types (i.e., metallicolous vs. nonmetallicolous). Also, approximate Bayesian computation analyses suggested that the current distribution of A. halleri in southern Poland could be relictual as a result of habitat fragmentation caused by climatic shifts during the Holocene, rather than due to recent colonization of industrially polluted sites. In addition, we find evidence that some nonmetallicolous lowland populations may have actually derived from metallicolous populations. Meanwhile, the distribution of quantitative variation in zinc hyperaccumulation did separate metallicolous and nonmetallicolous accessions, indicating more recent adaptive evolution and diversifying selection between metalliferous and nonmetalliferous habitats. This suggests that zinc hyperaccumulation evolves both ways-towards higher levels at nonmetalliferous sites and lower levels at metalliferous sites. Our results open a new perspective on possible evolutionary relationships between A. halleri edaphic types that may inspire future genetic studies of quantitative variation in metal hyperaccumulation.

When plants adapt to local environments, strong signatures of selection are expected in the genome, particularly in high-stress environments such as trace metal element enriched (metalliferous) soils. Using Arabidopsis halleri, a model species for metal homeostasis and adaptation to extreme environments, we identifid genes, gene variants, and pathways that are associated with soil properties and may thus contribute to adaptation to high concentrations of trace metal elements. We analysed whole-genome Pool-seq data from two metallicolous (from metalliferous soils) and two non-metallicolous populations (in total 119 individuals) and associated allele frequencies of the identified single-nucleotide polymorphisms (SNPs) with soil variables measured on site. Additionally, we accounted for polygenic adaptation by searching for gene pathways showing enrichment of signatures of selection. Out of >2.5 million SNPs, we identified 57 SNPs in 19 genes that were significantly associated with soil variables and are members of three enriched pathways. At least three of these candidate genes and pathways are involved in transmembrane transport and/or associated with responses to various stresses such as oxidative stress. We conclude that both allocation and detoxification processes play a crucial role in A. halleri for coping with these unfavourable conditions.

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Background and aims Pseudometallophytes are model organisms for adaptation and population differentiation because they persist in contrasting edaphic conditions of metalliferous and non-metalliferous habitats. We examine patterns of genetic divergence and local adaptation of Biscutella laevigata to assess historical and evolutionary processes shaping its genetic structure. Methods We sampled all known populations of B. laevigata in Poland and analyzed respective soil metal concentrations. For genotyping we used nine nuclear microsatellite loci. Population genetic pools were identified (Bayesian clustering) and we estimated genetic parameters and demographic divergence between metallicolous and non-metallicolous populations (ABCapproach). Results Populations clustered into two groups which corresponded to their edaphic origin and diverged 1,200 generations ago. We detected a significant decrease in genetic diversity and evidence for a recent bottleneck in metallicolous populations. Genetic structure was unrelated to site distribution but is rather influenced by environmental conditions (i.e. soil metal concentration). Conclusions The intriguing disjunctive distribution of B. laevigata in Poland results from a fragmentation of the species range during the Holocene, rather than recent long-distance-dispersal events. The genetic structure of populations, however, continues to be modified by microevolutionary processes at anthropogenic sites. These clear divergence patterns promote B. laevigata as a model species for plant adaptation to polluted environments.

The present study aimed to investigate phylogeographical patterns present within A. halleri in Central Europe, to propose hypotheses explaining the emergence of these patterns and to formulate hypotheses on the formation of the present day range of A. halleri in the region. 1281 accessions sampled from 52 populations within the investigated area were used in the study of genetic variation based on chloroplast DNA. Over 500 high quality species occurrence records were used in ecological niche modelling experiments. We evidenced the presence of a clear phylogeographic structure within A. halleri in Central Europe. Our results suggest that the species might have not survived the last glacial maximum in the Carpathians and Sudetes and that its range during the last glacial maximum might have consisted of at least two major parts: (1) a northern refugium consisting of vast refugial areas north and northeast of the Alps and (2) a southern refugium located in the Dinaric Alps and Balkan Mts. We postulate that the Sudetes and Western Carpathians were colonised mainly by plants originating from the northern refugium, whereas populations from the Eastern Carpathians originate from southern refugium. We also discuss our results in relation to the problematic taxonomy of the species.

The present study aimed to investigate phylogeographical patterns present within A.halleri in Central Europe, to propose hypotheses explaining the emergence of these patterns and to formulate hypotheses on the formation of the present day range of A.halleri in the region. 1281 accessions sampled from 52 populations within the investigated area were used in the study of genetic variation based on chloroplast DNA. Over 500 high quality species occurrence records were used in ecological niche modelling experiments.We evidenced the presence of a clear phylogeographic structure within A. halleri in Central Europe. Our results suggest that the species might have not survived the last glacial maximum in the Carpathians and Sudetes and that its range during the last glacial maximum might have consisted of at least two major parts: (1) a northern refugium consisting of vast refugial areas north and northeast of the Alps and (2) a southern refugium located in the Dinaric Alps and Balkan Mts. We postulate that the Sudetes and Western Carpathians were colonised mainly by plants originating from the northern refugium, whereas populations from the Eastern Carpathians originate from southern refugium. We also discuss our results in relation to the problematic taxonomy of the species. that its range during the last glacial maximum might have consisted of at least two major parts: 10(1) a northern refugium consisting of vast refugial areas north and northeast of the Alps and (2) a 11 southern refugium located in the Dinaric Alps and Balkan Mts. We postulate that the Sudetes and 12Western Carpathians were colonised mainly by plants originating from the northern refugium, 13whereas populations from the Eastern Carpathians originate from southern refugium. We also 14 discuss our results in relation to the problematic taxonomy of the species.

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The pseudometallophyte Biscutella laevigata adapts to metalliferous soils by allocating excess metal(loid)s to the endosperm (E) of seeds to protect embryonic tissues and improve reproductive success.