Secondary Evolution of a Self-Incompatibility Locus in the Brassicaceae Genus Leavenworthia

Sier-Ching Chantha (1) , Adam C Herman (1) , Adrian E Platts (1) , Xavier Vekemans (2) , Daniel J Schoen (1)

1 McGill University = Université McGill [Montréal, Canada]
2 GEPV - Laboratoire de Génétique et Evolution des Populations Végétales

Self-incompatibility (SI) is the flowering plant reproductive system in which self pollen tube growth is inhibited, thereby preventing self-fertilization. SI has evolved independently in several different flowering plant lineages. In all Brassicaceae species in which the molecular basis of SI has been investigated in detail, the product of the S-locus receptor kinase (SRK) gene functions as receptor in the initial step of the self pollen-rejection pathway, while that of the S-locus cysteine-rich (SCR) gene functions as ligand. Here we examine the hypothesis that the S locus in the Brassicaceae genus Leavenworthia is paralogous with the S locus previously characterized in other members of the family. We also test the hypothesis that self-compatibility in this group is based on disruption of the pollen ligand-producing gene. Sequence analysis of the S-locus genes in Leavenworthia, phylogeny of S alleles, gene expression patterns, and comparative genomics analyses provide support for both hypotheses. Of special interest are two genes located in a non-S locus genomic region of Arabidopsis lyrata that exhibit domain structures, sequences, and phylogenetic histories similar to those of the S-locus genes in Leavenworthia, and that also share synteny with these genes. These A. lyrata genes resemble those comprising the A. lyrata S locus, but they do not function in self-recognition. Moreover, they appear to belong to a lineage that diverged from the ancestral Brassicaceae S-locus genes before allelic diversification at the S locus. We hypothesize that there has been neo-functionalization of these S-locus-like genes in the Leavenworthia lineage, resulting in evolution of a separate ligand-receptor system of SI. Our results also provide support for theoretical models that predict that the least constrained pathway to the evolution of self-compatibility is one involving loss of pollen gene function. Citation: Chantha S-C, Herman AC, Platts AE, Vekemans X, Schoen DJ (2013) Secondary Evolution of a Self-Incompatibility Locus in the Brassicaceae Genus Leavenworthia. PLoS Biol 11(5): e1001560.

Mots clés: Abbreviations: SI; self-incompatibility; SC; self-compatibility; SCR; S-locus cysteine

Domaines: Génétique des populations [q-bio.PE]

Sier-Ching Chantha, Adam C Herman, Adrian E Platts, Xavier Vekemans, Daniel J Schoen. Secondary Evolution of a Self-Incompatibility Locus in the Brassicaceae Genus Leavenworthia. PLoS Biology, 2013, 11, pp.e1001560. ⟨10.1371/journal.pbio.1001560⟩. ⟨hal-01110802⟩