- ESE, CNRS University Paris Sud, Orsay, France
- Evolutionary genomics, Population genomics
Genetic mapping of sex and self-incompatibility determinants in the androdioecious plant Phillyrea angustifolia
Identification of distinct YX-like loci for sex determination and self-incompatibility in an androdioecious shrub
A wide variety of systems have evolved to control mating compatibility in sexual organisms. Their genetic determinism and the factors controlling their evolution represent fascinating questions in evolutionary biology and genomics. The plant Phillyrea angustifolia (Oleaeceae family) represents an exciting model organism, as it displays two distinct and rare mating compatibility systems : 1) males and hermaphrodites co-occur in populations of this shrub (a rare system called androdioecy), while the evolution and maintenance of purely hermaphroditic plants or mixtures of females and hermaphrodites (a system called gynodioecy) are easier to explain ; 2) a homomorphic diallelic self-incompatibility system acts in hermaphrodites, while such systems are usually multi-allelic, as rare alleles are advantageous, being compatible with all other alleles. Previous analyses of crosses brought some interesting answers to these puzzles, showing that males benefit from the ability to mate with all hermaphrodites regardless of their allele at the self-incompatibility system, and suggesting that both sex and self incompatibility are determined by XY-like genetic systems, i.e. with each a dominant allele; homozygotes for a single allele and heterozygotes therefore co-occur in natural populations at both sex and self-incompatibility loci .
Here, Carré et al. used genotyping-by-sequencing to build a genome linkage map of P. angustifolia . The elegant and original use of a probabilistic model of segregating alleles (implemented in the SEX-DETector method) allowed to identify both the sex and self-incompatibility loci , while this tool was initially developed for detecting sex-linked genes in species with strictly separated sexes (dioecy) . Carré et al.  confirmed that the sex and self-incompatibility loci are located in two distinct linkage groups and correspond to XY-like systems. A comparison with the genome of the closely related Olive tree indicated that their self-incompatibility systems were homologous. Such a XY-like system represents a rare genetic determination mechanism for self-incompatibility and has also been recently found to control mating types in oomycetes .
This study  paves the way for identifying the genes controlling the sex and self-incompatibility phenotypes and for understanding why and how self-incompatibility is only expressed in hermaphrodites and not in males. It will also be fascinating to study more finely the degree and extent of genomic differentiation at these two loci and to assess whether recombination suppression has extended stepwise away from the sex and self-incompatibility loci, as can be expected under some hypotheses, such as the sheltering of deleterious alleles near permanently heterozygous alleles . Furthermore, the co-occurrence in P. angustifolia of sex and mating types can contribute to our understanding of the factor controlling their evolution .
 Saumitou-Laprade P, Vernet P, Vassiliadis C, Hoareau Y, Magny G de, Dommée B, Lepart J (2010) A Self-Incompatibility System Explains High Male Frequencies in an Androdioecious Plant. Science, 327, 1648–1650. https://doi.org/10.1126/science.1186687
 Pannell JR, Voillemot M (2015) Plant Mating Systems: Female Sterility in the Driver’s Seat. Current Biology, 25, R511–R514. https://doi.org/10.1016/j.cub.2015.04.044
 Billiard S, Husse L, Lepercq P, Godé C, Bourceaux A, Lepart J, Vernet P, Saumitou-Laprade P (2015) Selfish male-determining element favors the transition from hermaphroditism to androdioecy. Evolution, 69, 683–693. https://doi.org/10.1111/evo.12613
 Carre A, Gallina S, Santoni S, Vernet P, Gode C, Castric V, Saumitou-Laprade P (2021) Genetic mapping of sex and self-incompatibility determinants in the androdioecious plant Phillyrea angustifolia. bioRxiv, 2021.04.15.439943, ver. 7 peer-reviewed and recommended by Peer Community in Genomics. https://doi.org/10.1101/2021.04.15.439943
 Muyle A, Käfer J, Zemp N, Mousset S, Picard F, Marais GA (2016) SEX-DETector: A Probabilistic Approach to Study Sex Chromosomes in Non-Model Organisms. Genome Biology and Evolution, 8, 2530–2543. https://doi.org/10.1093/gbe/evw172
 Dussert Y, Legrand L, Mazet ID, Couture C, Piron M-C, Serre R-F, Bouchez O, Mestre P, Toffolatti SL, Giraud T, Delmotte F (2020) Identification of the First Oomycete Mating-type Locus Sequence in the Grapevine Downy Mildew Pathogen, Plasmopara viticola. Current Biology, 30, 3897-3907.e4. https://doi.org/10.1016/j.cub.2020.07.057
 Jay P, Tezenas E, Giraud T (2021) A deleterious mutation-sheltering theory for the evolution of sex chromosomes and supergenes. bioRxiv, 2021.05.17.444504. https://doi.org/10.1101/2021.05.17.444504
 Billiard S, López-Villavicencio M, Devier B, Hood ME, Fairhead C, Giraud T (2011) Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types. Biological Reviews, 86, 421–442. https://doi.org/10.1111/j.1469-185X.2010.00153.x