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Pathways, ecological and genomic consequences of genome duplication in Arabidopsis arenosa, an overlooked diploid-polyploid member of the model genus Arabidopsis

Final Report Summary - WILD ARABIDOPSIS (Pathways, ecological and genomic consequences of genome duplication in Arabidopsis arenosa, an overlooked diploid-polyploid member of the model genus Arabidopsis)

Study aim
The plant genus Arabidopsis, including the leading model for genetic and evolutionary research A. thaliana, stands in main focus of science for over decades. In contrast to large information resources available for A. thaliana, other Arabidopsis species moved into focus of plant evolutionary biology only recently and, in particular, still little is known about diversity patterns in wild populations across their native distribution ranges.
The individual Marie Curie project WILDARABIDOPSIS was focused on the perhaps most diverse but least known member of the genus, Arabidopsis arenosa (sand rock-cress). This European species comprising populations of variable number of whole chromosome sets (diploid and autotetraploid) represents an emerging model for evolution through genome duplication (polyploidy). It also opens new avenues for study of habitat adaptation due to its large ecological amplitude spanning from coastal sand dunes and dry steppes in the foothills over rocks and screes on various substrates in mid-altitudes to alpine vegetation on the highest Carpathian summits. The project aimed to reveal the range-wide genetic structure of A. arenosa, trace potential genetic interactions among its two ploidy levels and assess the diversity of biologically important traits over various geographical areas and environments.

Key results
Based on an extensive sampling of natural populations and using high-throughput genotyping techniques (RAD sequencing) combined with eco-spatial analyses, we examined how the interplay of historical processes and niche shifts structured genetic diversity of Arabidopsis arenosa. Firstly, by focusing on diploid populations occupying poorly known parts of eastern and southern Europe the project documented previously unknown diversity (four spatio-ecologically distinct genetic lineages). The genetic makeup of current populations document important role of the Eastern-Central European mountains, not only as a harbor of unique diversity over last ice age(s) but also source for later expansion into novel high-altitude and high-latitude niches after the retreating glaciers. Specifically, while the traditionally-viewed harbor of temperate diversity in the Balkans hosted one isolated lineage of A. arenosa, most of its genetic diversity was concentrated further to the north in eastern Central Europe, where it likely survived the last ice age. In addition, two of the Central European lineages hybridized and the hybrid spread to a distinct postglacial environment in Northern Europe. The most prominent niche shifts were recorded for recently differentiated populations that expanded into narrowly defined alpine and northern coastal postglacial environments.
Further, we assessed the pathways and evolutionary consequences of origin of novel diversity via genome duplication (polyploidization). This work was based on a unique dataset of ~300 genomic sequences of A. arenosa of both ploidy levels across its range generated under newly established collaboration with Bomblies and Yant labs at John Innes Centre, Norwich, UK. So far, we observe frequent gene flow both within and across ploidy levels, which has likely a wide consequences for evolution of the group and its adaptive potential. An ongoing work is focused on identification of genomic regions under introgression and/or natural selection and revealing reasons for varying strength of both mechanisms in different environmental, ploidy and genetic contexts.

General significance
Wild Arabidopsis species are moving in focus of evolutionary biology and experimental science. Interpretation of the findings in a broad evolutionary framework is, however, still limited by largely missing background on their evolutionary history and range-wide genetic variation patterns. The WILDARABIDOPSIS project aimed to fill this gap by providing information about evolutionary history, structure of genetic diversity and phenotypic variation across entire distribution range of the highly variable species A. arenosa. This provides essential background knowledge and novel testable hypotheses to the Arabidopsis scientific community such as evolution of economically important genes in different genetic or ecological background. In summary, the project contributed to understanding role of environmental variation and genome duplication in genesis and maintenance of plant diversity and provided important background for follow-up studies focused on biodiversity conservation, agricultural and/or genetic applications.

Related scientific publications:
Kolar F, Fuxová G, Záveská E, Nagano AJ, Hyklová L, Lučanová M, Kudoh H, Marhold K (2016): Northern glacial refugia and altitudinal niche divergence shape genome-wide differentiation in the emerging plant model Arabidopsis arenosa. – Molecular Ecology, 25: 3929-49.

Contact details:
Filip Kolar, Natural History Museum, University of Oslo
current address: Department of Botany, Faculty of Science, Charles University in Prague, Benátská 2, 128 01, Praha 2, Czech Republic & Department of Flow Cytometry, Institute of Botany, Academy of Sciences, Zámek 1, 252 43, Průhonice, Czech Republic