(Mal)Adaptive consequences of inter-ploidy gene flow

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Genome duplication (polyploidisation) is a dominant force in sympatric speciation, particularly in plants including many crops. It is usually assumed that polyploidy poses an instant barrier to gene flow between diploid and its polyploid derivative. Our genomic survey, however, demonstrated rampant inter-ploidy gene flow in wild Arabidopsis. Yet mechanisms allowing such genome permeability and its evolutionary consequences remain elusive. In contrast to recent discoveries of ubiquity of gene flow in adaptation, we know little about this process in polyploids, mainly due to the technical challenges of polyploid population genomics. In this project, we aim to dissect drivers and mechanisms of ploidy barrier in five plant species and test the hypothesis that selection may promote inter-ploidy introgression. Firstly, we will infer mechanisms shaping inter-ploidy barrier by crossing experiments and transcriptomics. Then, we will test if selection shapes the differentiation landscape of admixed polyploid genomes using analysis of resequenced genomes from multiple natural contact zones. Finally, we will test whether gene flow from its diploid relatives could help the polyploid to gain additional variation and to establish itself in nature. The results have the potential to shift our perception of polyploidy towards speciation-with-gene-flow scenaria and inform breeding programmes involving polyploid crops.

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So far, we pioneered these questions in Arabidopsis arenosa. First, we detected rampant gene flow across previously assumed impermeable ploidy ‘barrier’ repeatedly in three regions (published recently in Nature Ecology and Evolution). We thus followed up by field and experimental inquiry of the strength and nature of such imperfect barrier. Using field sampling and flow cytometry of mixed-ploidy (2x+4x) populations across three natural ploidy contact zones we documented lack of triploid (3x) adult hybrids and two 3x seedlings germinated from in situ collected seeds. This is not due ecological separation as we found no distinction in local habitat preferences among the ploidies. To test whether such lack of hybrids is due to intrinsic barriers that take part after pollination we performed experimental crossings. Initial results confirmed that the majority (~90 %) of the inter-ploidy crossing progeny was triploid, although we also found a non-negligible proportion of tetraploid hybrids (~7 %), documenting the possible role of unreduced gametes in mediating gene flow. We confirmed reduced fertility of the interploidy crosses compared to the controls with respect to several measurements involving seed production and germination success. We used confocal microscopy and explored endosperm development in seeds produced from interploidy crosses (Fig.1). In contrast to normally developed controls, clear endosperm developmental defects were observed in both reciprocal interploidy crosses. These results document strong yet still incomplete triploid block in A. arenosa. Despite this, the complete absence of adult triploid hybrids in the field suggests alternative mechanisms of cross-ploidy gene flow such as involvement of unreduced gametes and formation of one-step tetraploid hybrids.

Funding: Czech Science Foundation (20-22783S)

Team members involved: Emma Morgan, Magdalena Lučanová, Martin Čertner

Key collaborators on this work are

Clement Lafon-Placette (Charles Univ. Prague)

Levi Yant (University of Nottingham, UK)

Mario Vallejo-Marín (University of Stirling, UK)

Kirsten Bomblies (ETH Zurich)

 

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