Clément Lafon-Placette, Ida M. Johannessen, Karina S. Hornslien, Mohammad F. Ali, Katrine N. Bjerkan, Jonathan Bramsiepe, Barbara M. Glöckle, Carolin A. Rebernig, Anne K. Brysting, Paul E. Grini, and Claudia Köhler

Significance

Hybrid seed lethality has been recognized and addressed by a long-standing tradition of plant-breeding research. Nevertheless, its role in evolution and speciation has been underestimated. In this study, hybrid seed lethality between Arabidopsis lyrata and Arabidopsis arenosa, two model species of growing interest in the scientific community, was investigated. This study shows that endosperm defects are sufficient to explain the direction of gene flow between the two wild species, suggesting an important role of this hybridization barrier in plant speciation. In addition, we show that natural polyploidization is involved in breaking down hybridization barriers, not only establishing them, as implied by the traditional “triploid block” concept. Our data suggest that polyploidy-mediated hybrid seed rescue, long known in artificial crosses, could play an important role in plant evolution.

Abstract

Based on the biological species concept, two species are considered distinct if reproductive barriers prevent gene flow between them. In Central Europe, the diploid species Arabidopsis lyrata and Arabidopsis arenosa are genetically isolated, thus fitting this concept as “good species.” Nonetheless, interspecific gene flow involving their tetraploid forms has been described. The reasons for this ploidy-dependent reproductive isolation remain unknown. Here, we show that hybridization between diploid A. lyrata and A. arenosa causes mainly inviable seed formation, revealing a strong postzygotic reproductive barrier separating these two species. Although viability of hybrid seeds was impaired in both directions of hybridization, the cause for seed arrest differed. Hybridization of A. lyrata seed parents with A. arenosa pollen donors resulted in failure of endosperm cellularization, whereas the endosperm of reciprocal hybrids cellularized precociously. Endosperm cellularization failure in both hybridization directions is likely causal for the embryo arrest. Importantly, natural tetraploid A. lyrata was able to form viable hybrid seeds with diploid and tetraploid A. arenosa, associated with the reestablishment of normal endosperm cellularization. Conversely, the defects of hybrid seeds between tetraploid A. arenosa and diploid A. lyrata were aggravated. According to these results, we hypothesize that a tetraploidization event in A. lyrata allowed the production of viable hybrid seeds with A. arenosa, enabling gene flow between the two species.

See: http://www.pnas.org/content/114/6/E1027.abstract

PNAS February 7 2017; vol. 114; no.6: E1027–E1035