Evolution of genomic imprinting in the Capsella genus

Abstract: According to the biological species concept, species are defined as groups of interbreeding populations reproductively isolated from other such groups. Hybrid seed lethality is a common reproductive barrier between plant species. Most frequently its developmental cause lies in the endosperm, but its molecular basis is not well understood. Hybrid seed defects differ depending on the cross direction, suggesting parent-of-origin-specific effects at work. Therefore, genomic imprinting, leading to the parent-of-origin-specific expression of genes in the endosperm, has been proposed to underlie hybrid seed lethality. Nevertheless, this hypothesis remains to be thoroughly tested. Therefore, the main goal of this thesis was to explore the link between genomic imprinting and hybrid seed lethality in Capsella. The first part of this work aimed at characterizing the imprintome (the set of imprinted genes) of Capsella rubella and to compare it with the imprintome of the closely related species Arabidopsis thaliana (10-14 million years apart). This revealed that the imprintomes of both species are poorly conserved. Nevertheless, the pathways regulating genomic imprinting target transposable elements (TEs) in both species. Furthermore, studying the imprintomes of three Capsella species supported the notion of poor imprinting conservation between related species. This work also revealed that imprintome divergence between Capsella species is based on the divergence of TE insertions and consequent silencing mechanisms. Furthermore, this work discovered that hybrid seed lethality is widespread between each of the Capsella species. This phenomenon originates in the endosperm and exhibits a parent-of-origin pattern. Importantly, this work revealed that endosperm-based hybridization barriers in Capsella correlate with the number and expression of paternally-expressed imprinted genes (PEGs). In addition, the mating system strongly impacts on the number of PEGs, which suggests that transitions of mating systems fuel the establishment of postzygotic hybridization barriers. Altogether, this thesis proposes a molecular and evolutionary explanation for the arising of endosperm-based hybridization barriers, in connection with genomic imprinting, TE dynamics and mating system. These data are expected to have a strong impact on plant breeding strategies and to promote further studies in this direction of research.

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