Sexual Dimorphism in White Campion: Complex Control of Carpel Number Is Revealed by Y Chromosome Deletions

Abstract

Sexual dimorphism in the dioecious plant white campion (Silene latifolia = Melandrium album) is under the control of two main regions on the Y chromosome. One such region, encoding the gynoecium-suppressing function (GSF), is responsible for the arrest of carpel initiation in male flowers. To generate chromosomal deletions, we used pollen irradiation in male plants to produce hermaphroditic mutants (bsx mutants) in which carpel development was restored. The mutants resulted from alterations in at least two GSF chromosomal regions, one autosomal and one located on the distal half of the (p)-arm of the Y chromosome. The two mutations affected carpel development independently, each mutation showing incomplete penetrance and variegation, albeit at significantly different levels. During successive meiotic generations, a progressive increase in penetrance and a reduction in variegation levels were observed and quantified at the level of the Y-linked GSF (GSF-Y). Possible mechanisms are proposed to explain the behavior of the bsx mutations: epigenetic regulation or/and second-site mutation of modifier genes. In addition, studies on the inheritance of the hermaphroditic trait showed that, unlike wild-type Y chromosomes, deleted Y chromosomes can be transmitted through both the male and the female lines. Altogether, these findings bring experimental support, on the one hand, to the existence on the Y chromosome of genic meiotic drive function(s) and, on the other hand, to models that consider that dioecy evolved through multiple mutation events. As such, the GSF is actually a system containing more than one locus and whose primary component is located on the Y chromosome.

Evolution of sex‐determination in dioecious plants: From active Y to X/A balance?

“…Early genetic work in S. latifolia has revealed the presence of two sex‐determining genes on the Y‐chromosome, the gynoecium suppressing factor ( GSF ) and stamen promoting factor ( SPF ). [ 4 ] The deletion of GSF or SPF sex‐determining genes leads to the development of hermaphroditic or asexual flowers, respectively, [ 14,15 ] which is consistent with the “two‐factor” model for sex determination and sex chromosome evolution. [ 5,6 ] Similarly, in asparagus and kiwifruit sex determination is controlled by two genes.…”

Labile sex expression in angiosperm species with sex chromosomes

“…Sex determination is considered quite stable in S. latifolia [88]. Completely monoclinous individuals (trioecy) have received some attention as they arise through deletions of parts of the Y chromosome and allow one to investigate the genetic architecture of dioecy in this species [2,71,89,90]. Leakiness does not seem to be caused by a mutation, at least in one report where it was found not to be heritable [91].…”

“…Some aberrant sexual phenotypes have been linked to mutations on the sex chromosomes and can be transmitted to descendants, as is often the case with trioecy (e.g. mutations on the Y chromosome in Carica papaya [96], Silene latifolia [71,89] and Vitis vinifera [97], or modified X chromosomes in Cannabis sativa [98] and Mercurialis annua [99]). One could hypothesize that leakiness, which involves only some flowers of a plant, is more often the result of 'developmental noise' [10] or of some local action of hormones than the other types of lability that involve whole plants and that might have genetic causes.…”

A CLAVATA3-like Gene Acts as a Gynoecium Suppression Function in White Campion

“…The work on genetics of sex determination and sex chromosomes in S. latifolia has played central role in the development of ideas in this research field ( Kejnovsky and Vyskot 2010 ; Charlesworth 2018 ). Classic cytogenetic and genetic work in S. latifolia has identified two regions on the Y-chromosome containing sex-determining genes: the gynoecium suppressing factor and the stamen promoting factor ( Westergaard 1946 ; Farbos et al 1999 ; Lardon et al 1999 ). The third Y-linked region responsible for anther maturation was also identified ( Westergaard 1946 ).…”