Evolution of sex determination and heterogamety changes in section Otites of the genus Silene

Abstract

Switches in heterogamety are known to occur in both animals and plants. Although plant sex determination systems probably often evolved more recently than those in several well-studied animals, including mammals, and have had less time for switches to occur, we previously detected a switch in heterogamety in the plant genus Silene: section Otites has both female and male heterogamety, whereas S. latifolia and its close relatives, in a different section of the genus, Melandrium (subgenus Behenantha), all have male heterogamety. Here we analyse the evolution of sex chromosomes in section Otites, which is estimated to have evolved only about 0.55 MYA. Our study confirms female heterogamety in S. otites and newly reveals female heterogamety in S. borysthenica. Sequence analyses and genetic mapping show that the sex-linked regions of these two species are the same, but the region in S. colpophylla, a close relative with male heterogamety, is different. The sex chromosome pairs of S. colpophylla and S. otites each correspond to an autosome of the other species, and both differ from the XY pair in S. latifolia. Silene section Otites species are suitable for detailed studies of the events involved in such changes, and our phylogenetic analysis suggests a possible change from female to male heterogamety within this section. Our analyses suggest a possibility that has so far not been considered, change in heterogamety through hybridization, in which a male-determining chromosome from one species is introgressed into another one, and over-rides its previous sex-determining system.

How to identify sex chromosomes and their turnover

“…However, whilst it was initially shown that organisms with a long haploid phase exhibit lower levels of sex chromosome divergence, including some algae (Ahmed et al, 2014) and plants (Bergero, Qiu, & Charlesworth, 2015;Chibalina & Filatov, 2011), a recent study using a larger data set of sex-linked genes found rapid degeneration of the Silene latifolia Y chromosome (Papadopulos, Chester, Ridout, & Filatov, 2015). This result, together with the observation that many plant clades exhibit turnover of sex chromosome systems (Balounova et al, 2019;Charlesworth, 2015;Martin et al, 2019;Moore, Harkess, & Weingartner, 2016;Tennessen et al, 2018), suggest that haploid selection might have a minimal effect on rates of Y degeneration.…”

“…In addition to turnover in the chromosome pair recruited to determine sex, transitions between different sex chromosome systems (e.g., XY to ZW, or ZW to XY) are also well documented across numerous clades. This diversity is particularly pronounced in certain groups of reptiles (Gamble et al, 2015;Pokorná & Kratochvíl, 2009), amphibians (Jeffries et al, 2018), fish Kitano & Peichel, 2012;Mank, Promislow, & Avise, 2006), insects (Blackmon & Demuth, 2014;Vicoso & Bachtrog, 2015) and plants (Balounova et al, 2019;Martin et al, 2019;Tennessen et al, 2018), where turnover between male (XY) and female (ZW) heterogamety is common over relatively short evolutionary time periods (Pennell et al, 2018). While recent efforts, including those of the Tree of Sex Consortium, have focused on characterizing the tremendous diversity of sex chromosomes across species, it is clear that we currently have an incomplete understanding of the variation in sex determination mechanisms across the tree of life Tree of Sex Consortium, 2014).…”

A General Model to Explain Repeated Turnovers of Sex Determination in the Salicaceae

“…For example, the sex chromosome turnover in strawberries is driven by repeated translocation of a female-specific sequence ( Tennessen et al. 2018 ); a heterogamety change from female to male was also proposed in section Otites of the genus Silene ( Balounova et al. 2019 ).…”

Chromosome‐scale assembly of the genome of Salixdunnii reveals a male‐heterogametic sex determination system on chromosome 7

“…Recent progress has included identifying sex‐linked regions in several plants with homomorphic sex chromosomes, and some of these have been found to be small parts of the chromosome pairs, allowing sex determining genes to be identified (e.g., Akagi et al, 2019 ; Harkess et al, 2017 , 2020 ; Müller et al, 2020 ; Zhou, Macaya‐Sanz, Carlson, et al, 2020 ); the genes are often involved in hormone response pathways, mainly associated with cytokinin and ethylene response pathways (reviewed by Feng et al, 2020 ). XX/XY (male heterogametic) and ZW/ZZ (female heterogametic) sex determination systems have been found in close relatives (Balounova et al, 2019 ; Martin et al, 2019 ; Müller et al, 2020 ; Zhou, Macaya‐Sanz, Carlson, et al, 2020 ). The extent to which related dioecious plants share the same sex‐determining systems, or evolved dioecy independently, is still not well understood, although there is accumulating evidence for independent evolution in the Salicaceae (Yang et al, 2020 ).…”