Evolutionary Strata on the X Chromosomes of the Dioecious Plant Silene latifolia: Evidence From New Sex-Linked Genes

Abstract

Despite its recent evolutionary origin, the sex chromosome system of the plant Silene latifolia shows signs of progressive suppression of recombination having created evolutionary strata of different X-Y divergence on sex chromosomes. However, even after 8 years of effort, this result is based on analyses of five sex-linked gene sequences, and the maximum divergence (and thus the age of this plant's sex chromosome system) has remained uncertain. More genes are therefore needed. Here, by segregation analysis of intron size variants (ISVS) and single nucleotide polymorphisms (SNPs), we identify three new Y-linked genes, one being duplicated on the Y chromosome, and test for evolutionary strata. All the new genes have homologs on the X and Y chromosomes. Synonymous divergence estimated between the X and Y homolog pairs is within the range of those already reported. Genetic mapping of the new X-linked loci shows that the map is the same in all three families that have been studied so far and that X-Y divergence increases with genetic distance from the pseudoautosomal region. We can now conclude that the divergence value is saturated, confirming the cessation of X-Y recombination in the evolution of the sex chromosomes at 10-20 MYA.

Rapid divergence and expansion of the X chromosome in papaya

“…The transposable element accumulation in the X-specific region is consistent with the greater quantity of such insertions in other sex chromosomes (X of mammals and Z of chickens) (14), and can be explained by its lower recombination frequency than that of autosomes; this difference arises because recombination occurs in only females, because of lack of recombination between the X-and Y-specific region in males (or HSY in hermaphrodites), in which the X spends one-third of its time. In Silene latifolia, whose sex chromosomes are extremely large and heteromorphic (the Y chromosome is 570 Mb and the X is 420 Mb), these changes have evolved over ∼10 million y (21). However, it is unclear if the S. latifolia sex chromosome pair is wholly derived from a single ancestral autosome.…”

Silene as a model system in ecology and evolution

“…The oldest stratum includes highly diverged genes that ceased recombining long ago, whereas genes in the youngest stratum are much less diverged (Lahn and Page, 1999). Over the last decade, several S. latifolia sex-linked genes have been identified (for example, Matsunaga et al, 2003;Filatov, 2005b), and they reveal that Silene sex chromosomes also have evolutionary strata with different divergence levels, indicating that recombination between these chromosomes also stopped in a step-wise manner over time (Nicolas et al, 2005;Bergero et al, 2007).…”

Expansion of the Pseudo-autosomal Region and Ongoing Recombination Suppression in the Silene latifolia Sex Chromosomes

“…Silene latifolia is a plant widely used for studying sex chromosome evolution, but the genetic map, even of its sex chromosomes, remains sparse (Bergero et al 2007) because, until recently, very few genes on these chromosomes had been identified. Those that have been mapped and sequenced from the X and Y demonstrate the existence of at least two evolutionary strata (Bergero et al 2007).…”

“…Those that have been mapped and sequenced from the X and Y demonstrate the existence of at least two evolutionary strata (Bergero et al 2007). Genic markers are preferable to anonymous ones such as AFLPs, the basis for the only previous dense genetic mapping in this species (Delph et al 2010), because codominant markers, such as SNPs and intron-size variants, are more reliable (e.g., Vekemans et al 2002) and allow integration of maps from both parents of a cross (e.g., Lorieux et al 1995a) and construction of consensus maps from multiple families.…”