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

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          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’.

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          Most cited references46

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          Scalable web services for the PSIPRED Protein Analysis Workbench

          Here, we present the new UCL Bioinformatics Group’s PSIPRED Protein Analysis Workbench. The Workbench unites all of our previously available analysis methods into a single web-based framework. The new web portal provides a greatly streamlined user interface with a number of new features to allow users to better explore their results. We offer a number of additional services to enable computationally scalable execution of our prediction methods; these include SOAP and XML-RPC web server access and new HADOOP packages. All software and services are available via the UCL Bioinformatics Group website at http://bioinf.cs.ucl.ac.uk/.
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            IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth.

            Plants are the principal source of iron in most diets, yet iron availability often limits plant growth. In response to iron deficiency, Arabidopsis roots induce the expression of the divalent cation transporter IRT1. Here, we present genetic evidence that IRT1 is essential for the uptake of iron from the soil. An Arabidopsis knockout mutant in IRT1 is chlorotic and has a severe growth defect in soil, leading to death. This defect is rescued by the exogenous application of iron. The mutant plants do not take up iron and fail to accumulate other divalent cations in low-iron conditions. IRT1-green fluorescent protein fusion, transiently expressed in culture cells, localized to the plasma membrane. We also show, through promoter::beta-glucuronidase analysis and in situ hybridization, that IRT1 is expressed in the external cell layers of the root, specifically in response to iron starvation. These results clearly demonstrate that IRT1 is the major transporter responsible for high-affinity metal uptake under iron deficiency.
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              Molecular mechanisms of plant metal tolerance and homeostasis.

              S Clemens (2001)
              Transition metals such as copper are essential for many physiological processes yet can be toxic at elevated levels. Other metals (e.g. lead) are nonessential and potentially highly toxic. Plants--like all other organisms--possess homeostatic mechanisms to maintain the correct concentrations of essential metal ions in different cellular compartments and to minimize the damage from exposure to nonessential metal ions. A regulated network of metal transport, chelation, trafficking and sequestration activities functions to provide the uptake, distribution and detoxification of metal ions. Some of the components of this network have now been identified: a number of uptake transporters have been cloned as well as candidate transporters for the vacuolar sequestration of metals. Chelators and chaperones are known, and evidence for intracellular metal trafficking is emerging. This recent progress in the molecular understanding of plant metal homeostasis and tolerance is reviewed.
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                Author and article information

                Journal
                Philos Trans R Soc Lond B Biol Sci
                Philos. Trans. R. Soc. Lond., B, Biol. Sci
                RSTB
                royptb
                Philosophical Transactions of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8436
                1471-2970
                22 July 2019
                3 June 2019
                3 June 2019
                : 374
                : 1777 , Theme issue ‘Convergent evolution in the genomics era: new insights and directions’ compiled and edited by Timothy B. Sackton and Nathan L. Clark
                : 20180243
                Affiliations
                [1 ]Molecular Genetics and Physiology of Plants, Faculty of Biology and Biotechnology, Ruhr University Bochum , 44801 Bochum, Germany
                [2 ]Cell and Developmental Biology, John Innes Centre , Norwich NR4 7UH, UK
                [3 ]School of Life Sciences, University of Nottingham , Nottingham NG7 2RD, UK
                Author notes

                One contribution of 16 to a theme issue ‘ Convergent evolution in the genomics era: new insights and directions’.

                [†]

                These authors contributed equally.

                [‡]

                Present address: Institute of Integrative Biology, ETH Zurich, 8092 Zurich, Switzerland.

                Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.4468805.

                Author information
                http://orcid.org/0000-0003-0070-0317
                http://orcid.org/0000-0001-7870-4508
                http://orcid.org/0000-0003-3442-0217
                Article
                rstb20180243
                10.1098/rstb.2018.0243
                6560266
                31154972
                721f316e-3239-485c-bdf1-3166ec50d71b
                © 2019 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 25 February 2019
                Funding
                Funded by: Biotechnology and Biological Sciences Research Council, http://dx.doi.org/10.13039/501100000268;
                Award ID: BB/P013511/1
                Funded by: Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung, http://dx.doi.org/10.13039/501100001711;
                Award ID: P2ZHP3_158773
                Funded by: Deutsche Forschungsgemeinschaft, http://dx.doi.org/10.13039/501100001659;
                Award ID: SPP1529 ADAPTOMICS (Kr1967/10-1 and -2)
                Award ID: SPP1819 RAPID EVOLUTION (Kr1967/16-1)
                Funded by: H2020 European Research Council, http://dx.doi.org/10.13039/100010663;
                Award ID: ERC-AdG 788380 LEAP-EXTREME
                Award ID: ERC-StG 679056 HOTSPOT
                Categories
                1001
                70
                197
                198
                204
                Part I: Population Genomics and Convergent Evolution within Species
                Research Article
                Custom metadata
                July 22, 2019

                Philosophy of science
                convergence,adaptation,evolution,selective sweep,selection
                Philosophy of science
                convergence, adaptation, evolution, selective sweep, selection

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