The Experts below are selected from a list of 360 Experts worldwide ranked by ideXlab platform

Nathalie Verbruggen - One of the best experts on this subject based on the ideXlab platform.

  • adaptation of Arabidopsis halleri to extreme metal pollution through limited metal accumulation involves changes in cell wall composition and metal homeostasis
    New Phytologist, 2021
    Co-Authors: Massimiliano Corso, Sol M Schvartzman, Eugeniusz Malkowski, Marc Hanikenne, Catherine Yvonne Jones, Veronica Gonzalezdoblas, William G T Willats, Nathalie Verbruggen
    Abstract:

    Metallophytes constitute powerful models for the study of metal homeostasis, adaptation to extreme environments and the evolution of naturally selected traits. Arabidopsis halleri is a pseudometallophyte which shows constitutive zinc/cadmium (Zn/Cd) tolerance and Zn hyperaccumulation but high intraspecific variability in Cd accumulation. To examine the molecular basis of the variation in metal tolerance and accumulation, ionome, transcriptome and cell wall glycan array profiles were compared in two genetically close A. halleri populations from metalliferous and nonmetalliferous sites in Northern Italy. The metallicolous population displayed increased tolerance to and reduced hyperaccumulation of Zn, and limited accumulation of Cd, as well as altered metal homeostasis, compared to the nonmetallicolous population. This correlated well with the differential expression of transporter genes involved in trace metal entry and in Cd/Zn vacuolar sequestration in roots. Many cell wall-related genes were also more highly expressed in roots of the metallicolous population. Glycan array and histological staining analyses demonstrated that there were major differences between the two populations in terms of the accumulation of specific root pectin and hemicellulose epitopes. Our results support the idea that both specific cell wall components and regulation of transporter genes play a role in limiting accumulation of metals in A. halleri at contaminated sites.

  • different strategies of cd tolerance and accumulation in Arabidopsis halleri and Arabidopsis arenosa
    Plant Cell and Environment, 2020
    Co-Authors: Michal Szopinski, Nathalie Verbruggen, Massimiliano Corso, Krzysztof Sitko, Szymon Rusinowski, Paulina Zieleźnikrusinowska, A Rostanski, Magdalena Rojekjelonek, Eugeniusz Malkowski
    Abstract:

    Pseudometallophytes are commonly used to study the evolution of metal tolerance and accumulation traits in plants. Within the Arabidopsis genus, the adaptation of Arabidopsis halleri to metalliferous soils has been widely studied, which is not the case for the closely related species Arabidopsis arenosa. We performed an in-depth physiological comparison between the A. halleri and A. arenosa populations from the same polluted site, together with the geographically close non-metallicolous (NM) populations of both species. The ionomes, growth, photosynthetic parameters and pigment content were characterized in the plants that were growing on their native site and in a hydroponic culture under Cd treatments. In situ, the metallicolous (M) populations of both species hyperaccumulated Cd and Zn. The NM population of A. halleri hyperaccumulated Cd and Zn while the NM A. arenosa did not. In the hydroponic experiments, the NM populations of both species accumulated more Cd in their shoots than the M populations. Our research suggests that the two Arabidopsis species evolved different strategies of adaptation to extreme metallic environments that involve fine regulation of metal homeostasis, adjustment of the photosynthetic apparatus and accumulation of flavonols and anthocyanins. This article is protected by copyright. All rights reserved.

  • cax1 suppresses cd induced generation of reactive oxygen species in Arabidopsis halleri
    Plant Cell and Environment, 2018
    Co-Authors: Hassan Ahmadi, Nathalie Verbruggen, Massimiliano Corso, M Weber, Stephan Clemens
    Abstract:

    The molecular analysis of metal hyperaccumulation in species such as Arabidopsis halleri offers the chance to gain insights into metal homeostasis and into the evolution of adaptation to extreme habitats. A prerequisite of metal hyperaccumulation is metal hypertolerance. Genetic analysis of a backcross population derived from Arabidopsis lyrata × A. halleri crosses revealed three quantitative trait loci for Cd hypertolerance. A candidate gene for Cdtol2 is AhCAX1, encoding a vacuolar Ca2+ /H+ antiporter. We developed a method for the transformation of vegetatively propagated A. halleri plants and generated AhCAX1-silenced lines. Upon Cd2+ exposure, several-fold higher accumulation of reactive oxygen species (ROS) was detectable in roots of AhCAX1-silenced plants. In accordance with the dependence of Cdtol2 on external Ca2+ concentration, this phenotype was exclusively observed in low Ca2+ conditions. The effects of external Ca2+ on Cd accumulation cannot explain the phenotype as they were not influenced by the genotype. Our data strongly support the hypothesis that higher expression of CAX1 in A. halleri relative to other Arabidopsis species represents a Cd hypertolerance factor. We propose a function of AhCAX1 in preventing a positive feedback loop of Cd-elicited ROS production triggering further Ca2+ -dependent ROS accumulation.

  • contrasting cadmium resistance strategies in two metallicolous populations of Arabidopsis halleri
    New Phytologist, 2018
    Co-Authors: Massimiliano Corso, Sol M Schvartzman, Flavia Guzzo, Florence Souard, Eugeniusz Malkowski, Marc Hanikenne, Nathalie Verbruggen
    Abstract:

    While cadmium (Cd) tolerance is a constitutive trait in the Arabidopsis halleri species, Cd accumulation is highly variable. Recent adaptation to anthropogenic metal stress has occurred independently within the genetic units of A. halleri and the evolution of different mechanisms involved in Cd tolerance and accumulation has been suggested. To gain a better understanding of the mechanisms underlying Cd tolerance and accumulation in A. halleri, ionomic inductively coupled plasma mass spectrometry (ICP-MS), transcriptomic (RNA sequencing) and metabolomic (high-performance liquid chromatography-mass spectrometry) profiles were analysed in two A. halleri metallicolous populations from different genetic units (PL22 from Poland and I16 from Italy). The PL22 and I16 populations were both hypertolerant to Cd, but PL22 hyperaccumulated Cd while I16 behaved as an excluder both in situ and when grown hydroponically. The observed hyperaccumulator vs excluder behaviours were paralleled by large differences in the expression profiles of transporter genes. Flavonoid-related transcripts and metabolites were strikingly more abundant in PL22 than in I16 shoots. The role of novel A. halleri candidate genes possibly involved in Cd hyperaccumulation or exclusion was supported by the study of corresponding A. thaliana knockout mutants. Taken together, our results are suggestive of the evolution of divergent strategies for Cd uptake, transport and detoxification in different genetic units of A. halleri.

  • adaptation to high zinc depends on distinct mechanisms in metallicolous populations of Arabidopsis halleri
    New Phytologist, 2018
    Co-Authors: Sol M Schvartzman, Nathalie Verbruggen, Massimiliano Corso, Nazeer Fataftah, Maxime Scheepers, Cecile Nouet, Bernard Bosman, Monique Carnol, Patrick Motte, Marc Hanikenne
    Abstract:

    Zinc (Zn) hyperaccumulation and hypertolerance are highly variable traits in Arabidopsis halleri. Metallicolous populations have evolved from nearby nonmetallicolous populations in multiple independent adaptation events. To determine whether these events resulted in similar or divergent adaptive strategies to high soil Zn concentrations, we compared two A. halleri metallicolous populations from distant genetic units in Europe (Poland (PL22) and Italy (I16)). The ionomic (Inductively Coupled Plasma Atomic Emission Spectroscopy (ICP-AES)) and transcriptomic (RNA sequencing (RNA-Seq)) responses to growth at 5 and 150 μM Zn were analyzed in root and shoot tissues to examine the contribution of the geographic origin and treatment to variation among populations. These analyses were enabled by the generation of a reference A. halleri transcriptome assembly. The genetic unit accounted for the largest variation in the gene expression profile, whereas the two populations had contrasting Zn accumulation phenotypes and shared little common response to the Zn treatment. The PL22 population displayed an iron deficiency response at high Zn in roots and shoots, which may account for higher Zn accumulation. By contrast, I16, originating from a highly Zn-contaminated soil, strongly responded to control conditions. Our data suggest that distinct mechanisms support adaptation to high Zn in soils among A. halleri metallicolous populations.

Pierre Saumitoulaprade - One of the best experts on this subject based on the ideXlab platform.

  • nuclear and chloroplast dna phylogeography reveals vicariance among european populations of the model species for the study of metal tolerance Arabidopsis halleri brassicaceae
    New Phytologist, 2012
    Co-Authors: Maxime Pauwels, Helene Frerot, Vincent Castric, Xavier Vekemans, Cécile Godé, Pierre Saumitoulaprade
    Abstract:

    Summary •Arabidopsis halleri is a pseudometallophyte involved in numerous molecular studies of the adaptation to anthropogenic metal stress. In order to test the representativeness of genetic accessions commonly used in these studies, we investigated the A. halleri population genetic structure in Europe. •Microsatellite and nucleotide polymorphisms from the nuclear and chloroplast genomes, respectively, were used to genotype 65 populations scattered over Europe. •The large-scale population structure was characterized by a significant phylogeographic signal between two major genetic units. The localization of the phylogeographic break was assumed to result from vicariance between large populations isolated in southern and central Europe, on either side of ice sheets covering the Alps during the Quaternary ice ages. Genetic isolation was shown to be maintained in western Europe by the high summits of the Alps, whereas admixture was detected in the Carpathians. •Considering the phylogeographic literature, our results suggest a distinct phylogeographic pattern for European species occurring in both mountain and lowland habitats. Considering the evolution of metal adaptation in A. halleri, it appears that recent adaptations to anthropogenic metal stress that have occurred within either phylogeographic unit should be regarded as independent events that potentially have involved the evolution of a variety of genetic mechanisms.

  • does speciation between Arabidopsis halleri and Arabidopsis lyrata coincide with major changes in a molecular target of adaptation
    PLOS ONE, 2011
    Co-Authors: Camille Roux, Vincent Castric, Maxime Pauwels, Pierre Saumitoulaprade, Stephen I Wright, Xavier Vekemans
    Abstract:

    Ever since Darwin proposed natural selection as the driving force for the origin of species, the role of adaptive processes in speciation has remained controversial. In particular, a largely unsolved issue is whether key divergent ecological adaptations are associated with speciation events or evolve secondarily within sister species after the split. The plant Arabidopsis halleri is one of the few species able to colonize soils highly enriched in zinc and cadmium. Recent advances in the molecular genetics of adaptation show that the physiology of this derived ecological trait involves copy number expansions of the AhHMA4 gene, for which orthologs are found in single copy in the closely related A. lyrata and the outgroup A. thaliana. To gain insight into the speciation process, we ask whether adaptive molecular changes at this candidate gene were contemporary with important stages of the speciation process. We first inferred the scenario and timescale of speciation by comparing patterns of variation across the genomic backgrounds of A. halleri and A. lyrata. Then, we estimated the timing of the first duplication of AhHMA4 in A. halleri. Our analysis suggests that the historical split between the two species closely coincides with major changes in this molecular target of adaptation in the A. halleri lineage. These results clearly indicate that these changes evolved in A. halleri well before industrial activities fostered the spread of Zn- and Cd-polluted areas, and suggest that adaptive processes related to heavy-metal homeostasis played a major role in the speciation process.

  • genetic architecture of zinc hyperaccumulation in Arabidopsis halleri the essential role of qtl environment interactions
    New Phytologist, 2010
    Co-Authors: Helene Frerot, Nathalie Verbruggen, Michel-pierre Faucon, G. Willems, C. Godé, A. Courseaux, A. Darracq, Pierre Saumitoulaprade
    Abstract:

    Summary •This study sought to determine the main genomic regions that control zinc (Zn) hyperaccumulation in Arabidopsis halleri and to examine genotype × environment effects on phenotypic variance. To do so, quantitative trait loci (QTLs) were mapped using an interspecific A. halleri × Arabidopsis lyrata petraea F2 population. •The F2 progeny as well as representatives of the parental populations were cultivated on soils at two different Zn concentrations. A linkage map was constructed using 70 markers. •In both low and high pollution treatments, zinc hyperaccumulation showed high broad-sense heritability (81.9 and 74.7%, respectively). Five significant QTLs were detected: two QTLs specific to the low pollution treatment (chromosomes 1 and 4), and three QTLs identified at both treatments (chromosomes 3, 6 and 7). These QTLs explained 50.1 and 36.5% of the phenotypic variance in low and high pollution treatments, respectively. Two QTLs identified at both treatments (chromosomes 3 and 6) showed significant QTL × environment interactions. •The QTL on chromosome 3 largely colocalized with a major QTL previously identified for Zn and cadmium (Cd) tolerance. This suggests that Zn tolerance and hyperaccumulation share, at least partially, a common genetic basis and may have simultaneously evolved on heavy metal-contaminated soils.

  • quantitative trait loci analysis of mineral element concentrations in an Arabidopsis halleri Arabidopsis lyrata petraea f2 progeny grown on cadmium contaminated soil
    New Phytologist, 2010
    Co-Authors: Glenda Willems, Helene Frerot, Pierre Saumitoulaprade, Jerome Gennen, Pietro Salis, Nathalie Verbruggen
    Abstract:

    Summary • This study describes the quantitative trait locus (QTL) analysis of cadmium (Cd), zinc (Zn), iron (Fe), potassium (K), magnesium (Mg) and calcium (Ca) accumulation in the pseudometallophyte Arabidopsis halleri under conditions of Cd excess using an interspecific A. halleri × Arabidopsis lyrata F2 population. • Our data provide evidence for the implication of one major QTL in Cd hyperaccumulation in A. halleri, and suggests that Cd tolerance and accumulation are not independent in A. halleri. Moreover, the major loci responsible for Zn hyperaccumulation in the absence of Cd appear to be the same when Cd is present at high concentrations. • More than twofold higher Fe concentrations were measured in A. halleri shoots than in A. lyrata, suggesting a different regulation of Fe accumulation in the hyperaccumulator. • With the exception of Ca, the accumulation of Cd was significantly correlated with the accumulation of all elements measured in the F2 progeny, suggesting pleiotropic gene action. However, QTL analysis identified pleiotropic QTLs only for Cd, Zn and Fe. Mg accumulation was negatively correlated with Cd accumulation, as well as with dry shoot biomass, suggesting that it might indicate cellular damage.

  • genomic pattern of adaptive divergence in Arabidopsis halleri a model species for tolerance to heavy metal
    Molecular Ecology, 2009
    Co-Authors: Clairelise Meyer, Pierre Saumitoulaprade, Renaud Vitalis, Vincent Castric
    Abstract:

    Pollution by heavy metals is one of the strongest environmental constraints in human-altered environments that only a handful of species can cope with. Identifying the genes conferring to those species the ability to grow in polluted areas is a first step towards a global understanding of the evolutionary processes involved and will eventually improve phytoremediation practices. We used a genome-scan approach to detect loci under divergent selection among four populations of Arabidopsis halleri growing on either polluted or nonpolluted habitats. Based on a high density of amplified fragment length polymorphism (AFLP) markers (820 AFLP markers, i.e. approximately 1 marker per 0.3Mb), evidence for selection was found for some markers in every sampled population. Four loci departed from neutrality in both metallicolous populations and thus constitute high-quality candidates for general adaptation to pollution. Interestingly, some candidates differed between the two metallicolous populations, suggesting the possibility that different loci may be involved in adaptation in the different metallicolous populations.

Ute Kramer - One of the best experts on this subject based on the ideXlab platform.

  • enhanced genome integrity maintenance and few directly stress mitigating alterations in extreme habitat adapted Arabidopsis halleri
    bioRxiv, 2020
    Co-Authors: Gwonjin Lee, Hassan Ahmadi, Veronica Preite, Lara Syllwasschy, Julia Quintana, Justin E Anderson, Bjorn Pietzenuk, Nadežda Janina, Ute Kramer
    Abstract:

    Abstract Heavy metal-rich toxic soils and ordinary soils are both natural habitats of Arabidopsis halleri, different from closely related plant species such as A. thaliana. Here we demonstrate enhanced Cd hypertolerance and attenuated Cd accumulation in plants originating from the most highly heavy metal-contaminated A. halleri site in Europe Ponte Nossa (Noss/IT), compared to A. halleri from non-metalliferous (NM) sites at both a small and a larger geographic distance. In the two populations from NM sites, hundreds of Cd-responsive transcripts mostly reflect the activation of Fe deficiency responses, whereas no single transcript responded to the same Cd treatment in plants from the metalliferous (M) site Noss. Instead, in Noss, thousands of transcripts exhibited an altered abundance irrespective of Cd exposure, with the highest enrichment for Gene Ontology Term “meiotic cell cycle”. Levels of ARGONAUTE 9 (AGO9) and the synaptonemal complex transverse filament protein-encoding ZYP1a/b transcripts, which are pre-meiosis- and meiosis-specific in A. thaliana, respectively, were strongly elevated in vegetative tissues of Noss, alongside transcripts with known additional functions in somatic genome integrity maintenance. Increased AGO9 transcript abundance was shared by individuals from M sites in Poland and Germany. Expression of IRON-REGULATED TRANSPORTER 1 (IRT1) was very low and of HEAVY METAL ATPASE 2 (HMA2) strongly elevated in Noss compared to both NM populations, largely explaining physiological differences in Cd handling. In summary, adaptation of Noss to extreme abiotic stress is associated with globally enhanced somatic genome integrity maintenance, as well as a small number of constitutive alterations in stress-specific functional networks.

  • enhanced genome integrity maintenance and few large stress mitigating changes in Arabidopsis halleri extreme habitat local adaptation
    bioRxiv, 2019
    Co-Authors: Gwonjin Lee, Hassan Ahmadi, Lara Syllwasschy, Julia Quintana, Justin E Anderson, Bjorn Pietzenuk, Ute Kramer
    Abstract:

    Abstract Heavy metal-rich toxic soils and ordinary soils are both natural habitats of Arabidopsis halleri, different from closely related plant species including A. thaliana. Here we demonstrate enhanced Cd hypertolerance and attenuated Cd accumulation in plants originating from the most highly heavy metal-contaminated A. halleri site in Europe at Ponte Nossa (Noss/IT), compared to A. halleri from non-metalliferous (NM) sites at a small and a larger phylogenetic distance. In the two populations from NM sites, hundreds of Cd-responsive transcripts mostly reflect the activation of Fe deficiency responses, whereas no single transcript showed differential abundance between Cd-exposed and untreated control plants from the metalliferous (M) site Noss. Among thousands of transcripts exhibiting between-population differential abundance in vegetative stage tissues, meiotic cell cycle functions were overrepresented, with an activation in plants from Noss. Between-population differences in transcript levels were highest for ARGONAUTE 9 (AGO9) and the synaptonemal complex transverse filament protein-encoding genes ZYP1a/b, which are pre-meiosis- and meiosis-specifically expressed, respectively, in A. thaliana. Moreover, transcript levels of IRON-REGULATED TRANSPORTER 1 (IRT1) were much lower in Noss and those of HEAVY METAL ATPASE 2 (HMA2) were far higher compared to both Pais and Wall, largely explaining between-population differences in Cd handling. Immunoblots for ZYP1 and IRT1 validated our observations at the protein level. In summary, plant adaptation to extreme abiotic stress is associated with globally enhanced somatic genome integrity maintenance including previously unsuspected gene functions, as well as a small number of constitutive alterations in stress-related functional networks. Significance Statement The re-establishment of ecosystems in extreme environments, which often arise through rapid anthropogenic change, relies on rare plants capable of colonizing such bare sites. As sessile organisms, these plants must possess effective physiological adaptations for coping with extraordinary abiotic stress levels, but the underlying molecular basis remains unknown. Here we examine intra-species transcriptomic divergence associated with an extreme-stress habitat, soil containing toxic levels of heavy metals, in somatic tissues of Arabidopsis halleri: Among activated biological processes, functions of the A. thaliana meiotic cell cycle are the most prominent, and we argue for their partly uncharacterized roles in genome integrity maintenance. Additionally, few but drastic differences in metal homeostasis gene expression largely explain environment-specific metal handling in different A. halleri populations.

  • Convergent evolution in Arabidopsis halleri and Arabidopsis arenosa on calamine metalliferous soils
    Philosophical transactions of the Royal Society of London. Series B Biological sciences, 2019
    Co-Authors: Veronica Preite, Ute Kramer, Hassan Ahmadi, Christian Sailer, Lara Syllwasschy, Sian Bray, Levi Yant
    Abstract:

    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. This article is part of the theme issue 'Convergent evolution in the genomics era: new insights and directions'.

  • real time whole plant dynamics of heavy metal transport in Arabidopsis halleri and Arabidopsis thaliana by gamma ray imaging
    Plant direct, 2019
    Co-Authors: Ute Kramer, Kaisa Kajala, Katherine L Walker, G S Mitchell, Simon R Cherry, Siobhan M Brady
    Abstract:

    Heavy metals such as zinc are essential for plant growth, but toxic at high concentrations. Despite our knowledge of the molecular mechanisms of heavy metal uptake by plants, experimentally addressing the real-time whole-plant dynamics of heavy metal uptake and partitioning has remained a challenge. To overcome this, we applied a high sensitivity gamma-ray imaging system to image uptake and transport of radioactive 65 Zn in whole-plant assays of Arabidopsis thaliana and the Zn hyperaccumulator Arabidopsis halleri. We show that our system can be used to quantitatively image and measure uptake and root-to-shoot translocation dynamics of zinc in real time. In the metal hyperaccumulator Arabidopsis halleri, 65 Zn uptake and transport from its growth media to the shoot occurs rapidly and on time scales similar to those reported in rice. In transgenic A. halleri plants in which expression of the zinc transporter gene HMA4 is suppressed by RNAi, 65 Zn uptake is completely abolished.

  • Supplementary methods from Convergent evolution in Arabidopsis halleri and Arabidopsis arenosa on calamine metalliferous soils
    2019
    Co-Authors: Veronica Preite, Ute Kramer, Hassan Ahmadi, Christian Sailer, Lara Syllwasschy, Sian Bray, Levi Yant
    Abstract:

    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’

Helene Frerot - One of the best experts on this subject based on the ideXlab platform.

  • Genetic architecture of a plant adaptive trait: QTL mapping of intraspecific variation for tolerance to metal pollution in Arabidopsis halleri
    Heredity, 2019
    Co-Authors: Marie-joe Karam, Maxime Pauwels, Marc Hanikenne, Julien Spielmann, Dima Souleman, M. Sol Schvartzman, Sophie Gallina, Charles Poncet, Olivier Bouchez, Helene Frerot
    Abstract:

    Anthropogenic activities are among the main drivers of global change and result in drastic habitat modifications, which represent strong evolutionary challenges for biological species that can either migrate, adapt, or disappear. In this context, understanding the genetics of adaptive traits is a prerequisite to enable long-term maintenance of populations under strong environmental constraints. To examine these processes, a QTL approach was developed here using the pseudometallophyte Arabidopsis halleri, which displays among-population adaptive divergence for tolerance to metallic pollution in soils. An F2 progeny was obtained by crossing individuals from metallicolous and non-metallicolous populations from Italian Alps, where intense metallurgic activities have created strong landscape heterogeneity. Then, we combined genome de novo assembly and genome resequencing of parental genotypes to obtain single-nucleotide polymorphism markers and achieve high-throughput genotyping of the progeny. QTL analysis was performed using growth parameters and photosynthetic yield to assess zinc tolerance levels. One major QTL was identified for photosynthetic yield. It explained about 27% of the phenotypic variance. Functional annotation of the QTL and gene expression analyses highlighted putative candidate genes. Our study represents a successful approach combining evolutionary genetics and advanced molecular tools, helping to better understand how a species can face new selective pressures of anthropogenic origin.

  • Habitat heterogeneity in the pseudometallophyte Arabidopsis halleri and its structuring effect on natural variation of zinc and cadmium hyperaccumulation
    Plant and Soil, 2017
    Co-Authors: Helene Frerot, Pierre Saumitou-laprade, Nina-coralie Hautekèete, Isabelle Decombeix, Marie-hélène Bouchet, Anne Créach, Yves Piquot, Maxime Pauwels
    Abstract:

    Arabidopsis halleri is a pseudometallophyte plant model hyperaccumulating zinc and cadmium. This study investigates which abiotic parameters may cause phenotypic divergence among accessions for hyperaccumulation traits. We studied 23 sites from a mining and industrial area in Italian Alps. Sites were characterized for altitude, topographic data, absolute humidity, and accompanying flora. Plant-soil couples were also sampled to measure shoot metal concentrations and soil elemental concentrations, particles size distribution, and pH. Using PLSR analyses, we investigated whether the natural variation in hyperaccumulation abilities could be explained by variation of abiotic parameters. Habitats heterogeneity was high, distinguishing metalliferous and non-metalliferous sites. However, heterogeneity was also observed for soil metal concentrations, particles size distribution and altitude, particularly among metalliferous habitats. This result was supported by floristic data. Soil zinc and cadmium concentrations showed the most contrasting effects on phenotypic divergence between metalliferous and non-metalliferous habitats. However, except for cadmium-related traits in non-metalliferous habitats, other abiotic parameters may affect the variation of zinc or cadmium hyperaccumulation within each habitat type. The classical dichotomous distinction between metalliferous and non-metalliferous habitats may hide the ecological diversity existing within each category for abiotic parameters. This study reveals abiotic parameters that may shape the natural variation of hyperaccumulation abilities.

  • nuclear and chloroplast dna phylogeography reveals vicariance among european populations of the model species for the study of metal tolerance Arabidopsis halleri brassicaceae
    New Phytologist, 2012
    Co-Authors: Maxime Pauwels, Helene Frerot, Vincent Castric, Xavier Vekemans, Cécile Godé, Pierre Saumitoulaprade
    Abstract:

    Summary •Arabidopsis halleri is a pseudometallophyte involved in numerous molecular studies of the adaptation to anthropogenic metal stress. In order to test the representativeness of genetic accessions commonly used in these studies, we investigated the A. halleri population genetic structure in Europe. •Microsatellite and nucleotide polymorphisms from the nuclear and chloroplast genomes, respectively, were used to genotype 65 populations scattered over Europe. •The large-scale population structure was characterized by a significant phylogeographic signal between two major genetic units. The localization of the phylogeographic break was assumed to result from vicariance between large populations isolated in southern and central Europe, on either side of ice sheets covering the Alps during the Quaternary ice ages. Genetic isolation was shown to be maintained in western Europe by the high summits of the Alps, whereas admixture was detected in the Carpathians. •Considering the phylogeographic literature, our results suggest a distinct phylogeographic pattern for European species occurring in both mountain and lowland habitats. Considering the evolution of metal adaptation in A. halleri, it appears that recent adaptations to anthropogenic metal stress that have occurred within either phylogeographic unit should be regarded as independent events that potentially have involved the evolution of a variety of genetic mechanisms.

  • genetic architecture of zinc hyperaccumulation in Arabidopsis halleri the essential role of qtl environment interactions
    New Phytologist, 2010
    Co-Authors: Helene Frerot, Nathalie Verbruggen, Michel-pierre Faucon, G. Willems, C. Godé, A. Courseaux, A. Darracq, Pierre Saumitoulaprade
    Abstract:

    Summary •This study sought to determine the main genomic regions that control zinc (Zn) hyperaccumulation in Arabidopsis halleri and to examine genotype × environment effects on phenotypic variance. To do so, quantitative trait loci (QTLs) were mapped using an interspecific A. halleri × Arabidopsis lyrata petraea F2 population. •The F2 progeny as well as representatives of the parental populations were cultivated on soils at two different Zn concentrations. A linkage map was constructed using 70 markers. •In both low and high pollution treatments, zinc hyperaccumulation showed high broad-sense heritability (81.9 and 74.7%, respectively). Five significant QTLs were detected: two QTLs specific to the low pollution treatment (chromosomes 1 and 4), and three QTLs identified at both treatments (chromosomes 3, 6 and 7). These QTLs explained 50.1 and 36.5% of the phenotypic variance in low and high pollution treatments, respectively. Two QTLs identified at both treatments (chromosomes 3 and 6) showed significant QTL × environment interactions. •The QTL on chromosome 3 largely colocalized with a major QTL previously identified for Zn and cadmium (Cd) tolerance. This suggests that Zn tolerance and hyperaccumulation share, at least partially, a common genetic basis and may have simultaneously evolved on heavy metal-contaminated soils.

  • quantitative trait loci analysis of mineral element concentrations in an Arabidopsis halleri Arabidopsis lyrata petraea f2 progeny grown on cadmium contaminated soil
    New Phytologist, 2010
    Co-Authors: Glenda Willems, Helene Frerot, Pierre Saumitoulaprade, Jerome Gennen, Pietro Salis, Nathalie Verbruggen
    Abstract:

    Summary • This study describes the quantitative trait locus (QTL) analysis of cadmium (Cd), zinc (Zn), iron (Fe), potassium (K), magnesium (Mg) and calcium (Ca) accumulation in the pseudometallophyte Arabidopsis halleri under conditions of Cd excess using an interspecific A. halleri × Arabidopsis lyrata F2 population. • Our data provide evidence for the implication of one major QTL in Cd hyperaccumulation in A. halleri, and suggests that Cd tolerance and accumulation are not independent in A. halleri. Moreover, the major loci responsible for Zn hyperaccumulation in the absence of Cd appear to be the same when Cd is present at high concentrations. • More than twofold higher Fe concentrations were measured in A. halleri shoots than in A. lyrata, suggesting a different regulation of Fe accumulation in the hyperaccumulator. • With the exception of Ca, the accumulation of Cd was significantly correlated with the accumulation of all elements measured in the F2 progeny, suggesting pleiotropic gene action. However, QTL analysis identified pleiotropic QTLs only for Cd, Zn and Fe. Mg accumulation was negatively correlated with Cd accumulation, as well as with dry shoot biomass, suggesting that it might indicate cellular damage.

Stephan Clemens - One of the best experts on this subject based on the ideXlab platform.

  • The two copies of the zinc and cadmium ZIP6 transporter of Arabidopsis halleri have distinct effects on cadmium tolerance
    Plant Cell and Environment, 2020
    Co-Authors: Julien Spielmann, Michael Weber, Hassan Ahmadi, Maxime Scheepers, Bernard Bosman, Monique Carnol, Patrick Motte, Sarah Nitsche, Juergen Kroymann, Stephan Clemens
    Abstract:

    Plants have the ability to colonize highly diverse environments. The zinc and cadmium hyperaccumulator Arabidopsis halleri has adapted to establish populations on soils covering an extreme range of metal availabilities. The A. halleri ZIP6 gene presents several hallmarks of hyperaccumulation candidate genes: it is constitutively highly expressed in roots and shoots and is associated with a zinc accumulation quantitative trait locus. Here, we show that AhZIP6 is duplicated in the A. halleri genome. The two copies are expressed mainly in the vasculature in both A. halleri and Arabidopsis thaliana, indicative of conserved cis regulation, and acquired partial organ specialization. Yeast complementation assays determined that AhZIP6 is a zinc and cadmium transporter. AhZIP6 silencing in A. halleri or expression in A. thaliana alters cadmium tolerance, but has no impact on zinc and cadmium accumulation. AhZIP6-silenced plants display reduced cadmium uptake upon short-term exposure, adding AhZIP6 to the limited number of Cd transporters supported by in planta evidence. Altogether, our data suggest that AhZIP6 is key to fine-tune metal homeostasis in specific cell types. This study additionally highlights the distinct fates of duplicated genes in A. halleri.

  • cax1 suppresses cd induced generation of reactive oxygen species in Arabidopsis halleri
    Plant Cell and Environment, 2018
    Co-Authors: Hassan Ahmadi, Nathalie Verbruggen, Massimiliano Corso, M Weber, Stephan Clemens
    Abstract:

    The molecular analysis of metal hyperaccumulation in species such as Arabidopsis halleri offers the chance to gain insights into metal homeostasis and into the evolution of adaptation to extreme habitats. A prerequisite of metal hyperaccumulation is metal hypertolerance. Genetic analysis of a backcross population derived from Arabidopsis lyrata × A. halleri crosses revealed three quantitative trait loci for Cd hypertolerance. A candidate gene for Cdtol2 is AhCAX1, encoding a vacuolar Ca2+ /H+ antiporter. We developed a method for the transformation of vegetatively propagated A. halleri plants and generated AhCAX1-silenced lines. Upon Cd2+ exposure, several-fold higher accumulation of reactive oxygen species (ROS) was detectable in roots of AhCAX1-silenced plants. In accordance with the dependence of Cdtol2 on external Ca2+ concentration, this phenotype was exclusively observed in low Ca2+ conditions. The effects of external Ca2+ on Cd accumulation cannot explain the phenotype as they were not influenced by the genotype. Our data strongly support the hypothesis that higher expression of CAX1 in A. halleri relative to other Arabidopsis species represents a Cd hypertolerance factor. We propose a function of AhCAX1 in preventing a positive feedback loop of Cd-elicited ROS production triggering further Ca2+ -dependent ROS accumulation.

  • relationships between soil and leaf mineral composition are element specific environment dependent and geographically structured in the emerging model Arabidopsis halleri
    New Phytologist, 2017
    Co-Authors: Ricardo J Stein, Stephan Clemens, Lara Syllwasschy, Stephan Horeth, Romario J F De Melo, Mario Luis Garbin, Ute Kramer
    Abstract:

    Summary Leaf mineral composition, the leaf ionome, reflects the complex interaction between a plant and its environment including local soil composition, an influential factor that can limit species distribution and plant productivity. Here we addressed within-species variation in plant–soil interactions and edaphic adaptation using Arabidopsis halleri, a well-suited model species as a facultative metallophyte and metal hyperaccumulator. We conducted multi-element analysis of 1972 paired leaf and soil samples from 165 European populations of A. halleri, at individual resolution to accommodate soil heterogeneity. Results were further confirmed under standardized conditions upon cultivation of 105 field-collected genotypes on an artificially metal-contaminated soil in growth chamber experiments. Soil-independent between- and within-population variation set apart leaf accumulation of zinc, cadmium and lead from all other nutrient and nonessential elements, concurring with differential hypothesized ecological roles in either biotic interaction or nutrition. For these metals, soil–leaf relationships were element-specific, differed between metalliferous and nonmetalliferous soils and were geographically structured both in the field and under standardized growth conditions, implicating complex scenarios of recent ecological adaptation. Our study provides an example and a reference for future related work and will serve as a basis for the molecular–genetic dissection and ecological analysis of the observed phenotypic variation.

  • between species differences in gene copy number are enriched among functions critical for adaptive evolution in Arabidopsis halleri
    BMC Genomics, 2016
    Co-Authors: Stephan Clemens, Michael Weber, Ute Kramer, Ina N. Talke, Vasantika Suryawanshi, Roland Eils, Benedikt Brors
    Abstract:

    Gene copy number divergence between species is a form of genetic polymorphism that contributes significantly to both genome size and phenotypic variation. In plants, copy number expansions of single genes were implicated in cultivar- or species-specific tolerance of high levels of soil boron, aluminium or calamine-type heavy metals, respectively. Arabidopsis halleri is a zinc- and cadmium-hyperaccumulating extremophile species capable of growing on heavy-metal contaminated, toxic soils. In contrast, its non-accumulating sister species A. lyrata and the closely related reference model species A. thaliana exhibit merely basal metal tolerance. For a genome-wide assessment of the role of copy number divergence (CND) in lineage-specific environmental adaptation, we conducted cross-species array comparative genome hybridizations of three plant species and developed a global signal scaling procedure to adjust for sequence divergence. In A. halleri, transition metal homeostasis functions are enriched twofold among the genes detected as copy number expanded. Moreover, biotic stress functions including mostly disease Resistance (R) gene-related genes are enriched twofold among genes detected as copy number reduced, when compared to the abundance of these functions among all genes. Our results provide genome-wide support for a link between evolutionary adaptation and CND in A. halleri as shown previously for Heavy metal ATPase4. Moreover our results support the hypothesis that elemental defences, which result from the hyperaccumulation of toxic metals, allow the reduction of classical defences against biotic stress as a trade-off.

  • isolation and characterization of Arabidopsis halleri and thlaspi caerulescens phytochelatin synthases
    Planta, 2011
    Co-Authors: Clairelise Meyer, Daniel Peisker, M Courbot, Adrian Radu Craciun, Anneclaire Cazale, Denis Desgain, Henk Schat, Stephan Clemens
    Abstract:

    The synthesis of phytochelatins (PC) represents a major metal and metalloid detoxification mechanism in various species. PC most likely play a role in the distribution and accumulation of Cd and possibly other metals. However, to date, no studies have investigated the phytochelatin synthase (PCS) genes and their expression in the Cd-hyperaccumulating species. We used functional screens in two yeast species to identify genes expressed by two Cd hyperaccumulators (Arabidopsis halleri and Thlaspi caerulescens) and involved in cellular Cd tolerance. As a result of these screens, PCS genes were identified for both species. PCS1 was in each case the dominating cDNA isolated. The deduced sequences of AhPCS1 and TcPCS1 are very similar to AtPCS1 and their identity is particularly high in the proposed catalytic N-terminal domain. We also identified in A. halleri and T. caerulescens orthologues of AtPCS2 that encode functional PCS. As compared to A. halleri and A. thaliana, T. caerulescens showed the lowest PCS expression. Furthermore, concentrations of PC in Cd-treated roots were the highest in A. thaliana, intermediate in A. halleri and the lowest in T. caerulescens. This mirrors the known capacity of these species to translocate Cd to the shoot, with T. caerulescens being the best translocator. Very low or undetectable concentrations of PC were measured in A. halleri and T. caerulescens shoots, contrary to A. thaliana. These results suggest that extremely efficient alternative Cd sequestration pathways in leaves of Cd hyperaccumulators prevent activation of PC synthase by Cd2+ ions.