A hemizygous supergene controls homomorphic and heteromorphic self-incompatibility systems in Oleaceae

Self-incompatibility (SI) has evolved independently multiple times and prevents self-fertilization in hermaphrodite angiosperms. Several groups of Oleaceae such as jasmines exhibit distylous flowers, with two compatibility groups each associated with a specific floral morph. 1 Green P.S. Oleaceae. in: Kadereit J.W. Flowering Plants · Dicotyledons: Lamiales (except Acanthaceae including Avicenniaceae). The Families and Genera of Vascular Plants. Springer, 2004: 296-306https://doi.org/10.1007/978-3-642-18617-2_16 Crossref Google Scholar Other Oleaceae species in the olive tribe have two compatibility groups without associated morphological variation. 2 De Cauwer I. Vernet P. Billiard S. Godé C. Bourceaux A. Ponitzki C. Saumitou-Laprade P. Widespread coexistence of self-compatible and self-incompatible phenotypes in a diallelic self-incompatibility system in Ligustrum vulgare (Oleaceae). Heredity. 2021; 127: 384-392https://doi.org/10.1038/s41437-021-00463-4 Crossref PubMed Scopus (6) Google Scholar ,3 Saumitou-Laprade P. Vernet P. Vassiliadis C. Hoareau Y. De Magny G. Dommée B. Lepart J. A self-incompatibility system explains high male frequencies in an androdioecious plant. Science. 2010; 327: 1648-1650https://doi.org/10.1126/science.1186687 Crossref PubMed Scopus (61) Google Scholar ,4 Saumitou-Laprade P. Vernet P. Vekemans X. Billiard S. Gallina S. Essalouh L. Mhaïs A. Moukhli A. El Bakkali A. Barcaccia G. et al. Elucidation of the genetic architecture of self-incompatibility in olive: evolutionary consequences and perspectives for orchard management. Evol. Appl. 2017; 10: 867-880https://doi.org/10.1111/eva.12457 Crossref PubMed Scopus (54) Google Scholar ,5 Vernet P. Lepercq P. Billiard S. Bourceaux A. Lepart J. Dommée B. Saumitou-Laprade P. Evidence for the long-term maintenance of a rare self-incompatibility system in Oleaceae. New Phytol. 2016; 210: 1408-1417https://doi.org/10.1111/nph.13872 Crossref PubMed Scopus (34) Google Scholar The genetic basis of both homomorphic and dimorphic SI systems in Oleaceae is unknown. By comparing genomic sequences of three olive subspecies (Olea europaea) belonging to the two compatibility groups, we first locate the genetic determinants of SI within a 700-kb hemizygous region present only in one compatibility group. We then demonstrate that the homologous hemizygous region also controls distyly in jasmine. Phylogenetic analyses support a common origin of both systems, following a segmental genomic duplication in a common ancestor. Examination of the gene content of the hemizygous region in different jasmine and olive species suggests that the mechanisms determining compatibility groups and floral phenotypes (whether homomorphic or dimorphic) in Oleaceae rely on the presence/absence of two genes involved in gibberellin and brassinosteroid regulation.