Preite_etal_2019_data.tar

This tar zipped folder contains the input and output files used for the genome scans described in the publication plus the SnpEff annotation data used

Adaptation to high soil trace metal element concentrations in Arabidopsis arenosa

Metalliferous soils are harsh environments for plants as a result of their low levels of macronutrients and richness in trace metal elements (TME; e.g. Cd, Pb, Zn). Plant survival under these conditions requires soil-specific adaptations. Arabidopsis arenosa, a relative of A. thaliana, is an obligate outcrosser that occurs on both metalliferous and non-metalliferous soils. We are interested in adaptive differences between populations from metalliferous (M) and non-metalliferous (NM) sites, from a genomic and a functional perspective. From natural M and NM populations, we collected leaves, soil and seeds of individual plants, determined leaf and soil TME content and performed genomic divergence scans and environmental association analyses. In a greenhouse reciprocal transplant experiment, we tested for local adaptation and differences in gene transcription (RNAseq). Further, to perform a bulked segregant analysis, we created a segregating F2 population by crossing M and NM individuals from one soil contrast. Here, we demonstrate that M populations are adapted to metalliferous soils and that metalliferous soils exert a strong selection pressure manifesting in differing survival rates of M and NM plants on metalliferous soil. We present how we identify candidate loci underlying adaptive differences between M and NM populations, by integrating population genomics (genome scans, association analyses), quantitative genetics (bulked segregant analysis, RNAseq) and in the near future molecular biology (cloning of alleles, characterisation of knock-out mutants). To date, our approach identified well characterised metal-adaptation genes (e.g. HMA4, MTP1) next to a majority of undescribed and (so far) non-metal related candidate loci

Convergent evolution in Arabidopsis halleri and Arabidopsis arenosa on calamine metalliferous soils

It is a plausible hypothesis that parallel adaptation events to the same environmental challenge should result in genetic changes of similar or identical effects, depending on the underlying fitness landscapes. However, systematic testing of this is scarce. Here we examine this hypothesis in two closely related plant species, Arabidopsis halleri and Arabidopsis arenosa, which co-occur at two calamine metalliferous (M) sites harbouring toxic levels of the heavy metals zinc and cadmium. We conduct individual genome resequencing alongside soil elemental analysis for 64 plants from eight populations on M and non-metalliferous (NM) soils, and identify genomic footprints of selection and local adaptation. Selective sweep and environmental association analyses indicate a modest degree of gene as well as functional network convergence, whereby the proximal molecular factors mediating this convergence mostly differ between site pairs and species. Notably, we observe repeated selection on identical single nucleotide polymorphisms in several A. halleri genes at two independently colonized M sites. Our data suggest that species-specific metal handling and other biological features could explain a low degree of convergence between species. The parallel establishment of plant populations on calamine M soils involves convergent evolution, which will probably be more pervasive across sites purposely chosen for maximal similarity in soil composition.ISSN:1471-2970ISSN:0962-843

Convergent evolution in<i>Arabidopsis halleri</i>and<i>Arabidopsis arenosa</i>on calamine metalliferous soils

It is a plausible hypothesis that parallel adaptation events to the same environmental challenge should result in genetic changes of similar or identical effects, depending on the underlying fitness landscapes. However, systematic testing of this is scarce. Here we examine this hypothesis in two closely related plant species,Arabidopsis halleriandArabidopsis arenosa, which co-occur at two calamine metalliferous (M) sites harbouring toxic levels of the heavy metals zinc and cadmium. We conduct individual genome resequencing alongside soil elemental analysis for 64 plants from eight populations on M and non-metalliferous (NM) soils, and identify genomic footprints of selection and local adaptation. Selective sweep and environmental association analyses indicate a modest degree of gene as well as functional network convergence, whereby the proximal molecular factors mediating this convergence mostly differ between site pairs and species. Notably, we observe repeated selection on identical single nucleotide polymorphisms in severalA. hallerigenes at two independently colonized M sites. Our data suggest that species-specific metal handling and other biological features could explain a low degree of convergence between species. The parallel establishment of plant populations on calamine M soils involves convergent evolution, which will probably be more pervasive across sites purposely chosen for maximal similarity in soil composition.This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’.</jats:p

Constitutively enhanced genome integrity maintenance and direct stress mitigation characterize transcriptome of extreme stress-adapted<i>Arabidopsis halleri</i>

AbstractHeavy metal-rich toxic soils and ordinary soils are both natural habitats ofArabidopsis halleri. The molecular divergence underlying survival in sharply contrasting environments is unknown. Here we comparatively address metal physiology and transcriptomes ofA. hallerioriginating from the most highly heavy metal-contaminated soil in Europe, Ponte Nossa (Noss/IT), and from non-metalliferous (NM) soil. Noss exhibits enhanced hypertolerance and attenuated accumulation of cadmium (Cd), and transcriptomic Cd responsiveness is decreased, compared to plants of NM soil origin. Among the condition-independent transcriptome characteristics of Noss, the most highly overrepresented functional class of “meiotic cell cycle” comprises 21 transcripts with elevated abundance in vegetative tissues, in particularArgonaute 9(AGO9) and the synaptonemal complex transverse filament protein-encodingZYP1a/b. IncreasedAGO9transcript levels in Noss are accompanied by decreased long terminal repeat retrotransposon expression, and are shared by plants from milder metalliferous sites in Poland and Germany. Expression ofIron-regulated Transporter(IRT1) is very low and ofHeavy Metal ATPase 2(HMA2) strongly elevated in Noss, which can account for its specific Cd handling. In plants adapted to the most extreme abiotic stress, broadly enhanced functions comprise genes with likely roles in somatic genome integrity maintenance, accompanied by few alterations in stress-specific functional networks.</jats:p

Figure S3 from Convergent evolution in <i>Arabidopsis halleri</i> and <i>Arabidopsis arenosa</i> on calamine metalliferous soils

It is a plausible hypothesis that parallel adaptation events to the same environmental challenge should result in genetic changes of similar or identical effects, depending on the underlying fitness landscapes. However, systematic testing of this is scarce. Here we examine this hypothesis in two closely related plant species, Arabidopsis halleri and Arabidopsis arenosa, which co-occur at two calamine metalliferous sites harbouring toxic levels of the heavy metals zinc and cadmium. We conduct individual genome resequencing alongside soil elemental analysis for 64 plants from eight populations on metalliferous and non-metalliferous soils, and identify genomic footprints of selection and local adaptation. Selective sweep and environmental association analyses indicate a modest degree of gene as well as functional network convergence, whereby the proximal molecular factors mediating this convergence mostly differ between site pairs and species. Notably, we observe repeated selection on identical SNPs in several A. halleri genes at two independently colonized metalliferous sites. Our data suggest that species-specific metal handling and other biological features could explain a low degree of convergence between species. The parallel establishment of plant populations on calamine metalliferous soils involves convergent evolution, which will likely be more pervasive across sites purposely chosen for maximal similarity in soil composition.This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’

Figure S2 from Convergent evolution in <i>Arabidopsis halleri</i> and <i>Arabidopsis arenosa</i> on calamine metalliferous soils

It is a plausible hypothesis that parallel adaptation events to the same environmental challenge should result in genetic changes of similar or identical effects, depending on the underlying fitness landscapes. However, systematic testing of this is scarce. Here we examine this hypothesis in two closely related plant species, Arabidopsis halleri and Arabidopsis arenosa, which co-occur at two calamine metalliferous (M) sites harbouring toxic levels of the heavy metals zinc and cadmium. We conduct individual genome resequencing alongside soil elemental analysis for 64 plants from eight populations on M and non-metalliferous (NM) soils, and identify genomic footprints of selection and local adaptation. Selective sweep and environmental association analyses indicate a modest degree of gene as well as functional network convergence, whereby the proximal molecular factors mediating this convergence mostly differ between site pairs and species. Notably, we observe repeated selection on identical single nucleotide poly-morphisms in several A. halleri genes at two independently colonized M sites. Our data suggest that species-specific metal handling and other biological features could explain a low degree of convergence between species. The parallel establishment of plant populations on calamine M soils involves convergent evolution, which will probably be more pervasive across sites purposely chosen for maximal similarity in soil composition.This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’

Figure S1 from Convergent evolution in <i>Arabidopsis halleri</i> and <i>Arabidopsis arenosa</i> on calamine metalliferous soils

It is a plausible hypothesis that parallel adaptation events to the same environmental challenge should result in genetic changes of similar or identical effects, depending on the underlying fitness landscapes. However, systematic testing of this is scarce. Here we examine this hypothesis in two closely related plant species, Arabidopsis halleri and Arabidopsis arenosa, which co-occur at two calamine metalliferous (M) sites harbouring toxic levels of the heavy metals zinc and cadmium. We conduct individual genome resequencing alongside soil elemental analysis for 64 plants from eight populations on M and non-metalliferous (NM) soils, and identify genomic footprints of selection and local adaptation. Selective sweep and environmental association analyses indicate a modest degree of gene as well as functional network convergence, whereby the proximal molecular factors mediating this convergence mostly differ between site pairs and species. Notably, we observe repeated selection on identical single nucleotide poly-morphisms in several A. halleri genes at two independently colonized M sites. Our data suggest that species-specific metal handling and other biological features could explain a low degree of convergence between species. The parallel establishment of plant populations on calamine M soils involves convergent evolution, which will probably be more pervasive across sites purposely chosen for maximal similarity in soil composition.This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’

Constitutively enhanced genome integrity maintenance and direct stress mitigation characterize transcriptome of extreme stress-adapted Arabidopsis halleri

16 Pág.Heavy metal-rich toxic soils and ordinary soils are both natural habitats of Arabidopsis halleri, a diploid perennial and obligate outcrosser in the sister clade of the genetic model plant Arabidopsis thaliana. The molecular divergence underlying survival in sharply contrasting environments is unknown. Here we comparatively address metal physiology and transcriptomes of A. halleri originating from the most highly heavy metal-contaminated soil in Europe, Ponte Nossa, Italy (Noss), and from non-metalliferous (NM) soils. Plants from Noss exhibit enhanced hypertolerance and attenuated accumulation of cadmium (Cd), and their transcriptomic Cd responsiveness is decreased, compared to plants of NM soil origin. Among the condition-independent transcriptome characteristics of Noss, the most highly overrepresented functional class of 'meiotic cell cycle' comprises 21 transcripts with elevated abundance in vegetative tissues, in particular Argonaute 9 (AGO9) and the synaptonemal complex transverse filament protein-encoding ZYP1a/b. Increased AGO9 transcript levels in Noss are accompanied by decreased long terminal repeat retrotransposon expression. Similar to Noss, plants from other highly metalliferous sites in Poland and Germany share elevated somatic AGO9 transcript levels in comparison to plants originating from NM soils in their respective geographic regions. Transcript levels of Iron-Regulated Transporter 1 (IRT1) are very low and transcript levels of Heavy Metal ATPase 2 (HMA2) are strongly elevated in Noss, which can account for its altered Cd handling. We conclude that in plants adapted to the most extreme abiotic stress, broadly enhanced functions comprise genes with likely roles in somatic genome integrity maintenance, accompanied by few alterations in stress-specific functional networks.This work was supported by the Deutsche Forschungsgemeinschaft (Research Priority Program SPP1529 ADAPTOMICS, start-up grant to GL and JEA from grant number Kr1967/12 to UK; Research Priority Program SPP1819 RAPID EVOLUTION, grant number Kr1967/16 to UK; and individual grant Kr1967/3-3 to UK) and a European Research Council Advanced Grant (grant number 788380 to UK). We acknowledge the Bielefeld-Giessen Center for Microbial Bioinformatics (BiGi) of the German Federal Ministry of Education and the Research-funded German network for bioinformatics infrastructure (de.NBI, grant 031A533) for providing computational resources and related general support.Peer reviewe