The slowdown of Y chromosome expansion in dioecious Silene latifolia due to DNA loss and male-specific silencing of retrotransposons

Abstract

BackgroundThe rise and fall of the Y chromosome was demonstrated in animals but plants often possess the large evolutionarily young Y chromosome that is thought has expanded recently. Break-even points dividing expansion and shrinkage phase of plant Y chromosome evolution are still to be determined. To assess the size dynamics of the Y chromosome, we studied intraspecific genome size variation and genome composition of male and female individuals in a dioecious plant Silene latifolia, a well-established model for sex-chromosomes evolution.ResultsOur genome size data are the first to demonstrate that regardless of intraspecific genome size variation, Y chromosome has retained its size in S. latifolia. Bioinformatics study of genome composition showed that constancy of Y chromosome size was caused by Y chromosome DNA loss and the female-specific proliferation of recently active dominant retrotransposons. We show that several families of retrotransposons have contributed to genome size variation but not to Y chromosome size change.ConclusionsOur results suggest that the large Y chromosome of S. latifolia has slowed down or stopped its expansion. Female-specific proliferation of retrotransposons, enlarging the genome with exception of the Y chromosome, was probably caused by silencing of highly active retrotransposons in males and represents an adaptive mechanism to suppress degenerative processes in the haploid stage. Sex specific silencing of transposons might be widespread in plants but hidden in traditional hermaphroditic model plants.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4547-7) contains supplementary material, which is available to authorized users.

Degenerative Expansion of a Young Supergene

“…Intriguingly, the supergene region of suppressed recombination on the hermaphrodite determining Y h chromosome of papaya (7 million years old, i.e., ∼7 million generations) is approximately 2-fold larger than the homologous region in the X chromosome (Wang et al 2012). Such findings of size increases in nonrecombining sex chromosomes suggest that large-scale accumulation of repetitive elements could precede gene loss (Hobza et al 2017; Puterova et al 2018). However, there are no convincing demonstrations of how or when such “degenerative expansion” occurs (Ming et al 2007) in animals.…”

Early Sex-Chromosome Evolution in the Diploid Dioecious PlantMercurialis annua

“…Early sex-chromosome evolution typically involves the accumulation of repetitive sequences in a nonrecombining region (J. Wang et al 2012; Hobza et al 2017), differences in codon use between homologs (Ono 1939; Qiu et al 2010), different patterns of gene expression at sex-linked loci (Zemp et al 2016), pseudogenization and gene loss (Papadopulos et al 2015; Wu and Moore 2015), and, ultimately, divergence in chromosome length between homologs (Puterova et al 2018). Extreme divergence is common in many animals, but it is also known in some plants in which the homologous chromosomes are heteromorphic and distinguishable by karyotype, e.g.…”

Retrotransposons in Plant Genomes: Structure, Identification, and Classification through Bioinformatics and Machine Learning

“…Sex chromosomes are known to accumulate repetitive sequences [80] due to suppression of recombination, but the sex-specific accumulation of transposable elements could also contribute to the differential repeat content of the X and Y chromosomes (the Y chromosome is larger than the X chromosome in Silene latifolia ). This fact leads to size variation [147] in many reported genomes, such as sea buckthorn [148], papaya [149,150], Silene latifolia , Coccinia grandis and Cannabis sativa [124], as well as to other mechanisms that vary in dioecious species, such as population size and genome dynamics [148]. Further, TEs could be responsible for a lower gene content in the Y chromosome of S. latifolia (although the Y chromosome is the largest in this species and is ~1.4 times larger than the X chromosome [147]).…”