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Role of ploidy in colonization of alpine habitats in natural populations of Arabidopsis arenosa.

ABSTRACT: BACKGROUND AND AIMS:Polyploidy is an important driver of plant diversification and adaptation to novel environments. As a consequence of genome doubling, polyploids often exhibit greater colonizing ability or occupy a wider ecological niche than diploids. Although elevation has been traditionally considered as a key driver structuring ploidy variation, we do not know if environmental and phenotypic differentiation among ploidy cytotypes varies along an elevational gradient. Here, we tested for the consequences of genome duplication on genetic diversity, phenotypic variation and habitat preferences on closely related diploid and tetraploid populations that coexist along approx. 2300 m of varying elevation. METHODS:We sampled and phenotyped 45 natural diploid and tetraploid populations of Arabidopsis arenosa in one mountain range in Central Europe (Western Carpathians) and recorded abiotic and biotic variables at each collection site. We inferred genetic variation, population structure and demographic history in a sub-set of 29 populations genotyped for approx. 36 000 single nucleotide polymorphisms. KEY RESULTS:We found minor effects of polyploidy on colonization of alpine stands and low genetic differentiation between the two cytotypes, mirroring recent divergence of the polyploids from the local diploid lineage and repeated reticulation events among the cytotypes. This pattern was corroborated by the absence of ecological niche differentiation between the two cytotypes and overall phenotypic similarity at a given elevation. CONCLUSIONS:The case of A. arenosa contrasts with previous studies that frequently showed clear niche differentiation between cytotypes. Our work stresses the importance of considering genetic structure and past demographic processes when interpreting the patterns of ploidy distributions, especially in species that underwent recent polyploidization events.

SUBMITTER: Wos G

PROVIDER: S-EPMC6758580 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Role of ploidy in colonization of alpine habitats in natural populations of Arabidopsis arenosa.

Wos Guillaume G Mořkovská Jana J Bohutínská Magdalena M Šrámková Gabriela G Knotek Adam A Lučanová Magdalena M Španiel Stanislav S Marhold Karol K Kolář Filip F

Annals of botany 20190901 2

<h4>Background and aims</h4>Polyploidy is an important driver of plant diversification and adaptation to novel environments. As a consequence of genome doubling, polyploids often exhibit greater colonizing ability or occupy a wider ecological niche than diploids. Although elevation has been traditionally considered as a key driver structuring ploidy variation, we do not know if environmental and phenotypic differentiation among ploidy cytotypes varies along an elevational gradient. Here, we test ...[more]

PMID: 31185073

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Project description:Genome duplication, which results in polyploidy, is disruptive to fundamental biological processes. Genome duplications occur spontaneously in a range of taxa and problems such as sterility, aneuploidy, and gene expression aberrations are common in newly formed polyploids. In mammals, genome duplication is associated with cancer and spontaneous abortion of embryos. Nevertheless, stable polyploid species occur in both plants and animals. Understanding how natural selection enabled these species to overcome early challenges can provide important insights into the mechanisms by which core cellular functions can adapt to perturbations of the genomic environment. Arabidopsis arenosa includes stable tetraploid populations and is related to well-characterized diploids A. lyrata and A. thaliana. It thus provides a rare opportunity to leverage genomic tools to investigate the genetic basis of polyploid stabilization. We sequenced the genomes of twelve A. arenosa individuals and found signatures suggestive of recent and ongoing selective sweeps throughout the genome. Many of these are at genes implicated in genome maintenance functions, including chromosome cohesion and segregation, DNA repair, homologous recombination, transcriptional regulation, and chromatin structure. Numerous encoded proteins are predicted to interact with one another. For a critical meiosis gene, ASYNAPSIS1, we identified a non-synonymous mutation that is highly differentiated by cytotype, but present as a rare variant in diploid A. arenosa, indicating selection may have acted on standing variation already present in the diploid. Several genes we identified that are implicated in sister chromatid cohesion and segregation are homologous to genes identified in a yeast mutant screen as necessary for survival of polyploid cells, and also implicated in genome instability in human diseases including cancer. This points to commonalities across kingdoms and supports the hypothesis that selection has acted on genes controlling genome integrity in A. arenosa as an adaptive response to genome doubling.

Dataset Information

Role of ploidy in colonization of alpine habitats in natural populations of Arabidopsis arenosa.

Publications

Role of ploidy in colonization of alpine habitats in natural populations of Arabidopsis arenosa.

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