Multiple gene movements into and out of haploid sex chromosomes

Agnieszka P Lipinska,Akira F Peters,Susana M Coelho,J Mark Cock,Svenja Heesch,Nicholas R T Toda

doi:10.1186/s13059-017-1201-7

Abstract

BackgroundLong-term evolution of sex chromosomes is a dynamic process shaped by gene gain and gene loss. Sex chromosome gene traffic has been studied in XY and ZW systems but no detailed analyses have been carried out for haploid phase UV sex chromosomes. Here, we explore sex-specific sequences of seven brown algal species to understand the dynamics of the sex-determining region (SDR) gene content across 100 million years of evolution.ResultsA core set of sex-linked genes is conserved across all the species investigated, but we also identify modifications of both the U and the V SDRs that occurred in a lineage-specific fashion. These modifications involve gene loss, gene gain and relocation of genes from the SDR to autosomes. Evolutionary analyses suggest that the SDR genes are evolving rapidly and that this is due to relaxed purifying selection. Expression analysis indicates that genes that were acquired from the autosomes have been retained in the SDR because they confer a sex-specific role in reproduction. By examining retroposed genes in Saccharina japonica, we demonstrate that UV sex chromosomes have generated a disproportionate number of functional orphan retrogenes compared with autosomes. Movement of genes out of the UV sex chromosome could be a means to compensate for gene loss from the non-recombining region, as has been suggested for Y-derived retrogenes in XY sexual systems.ConclusionThis study provides the first analysis of gene traffic in a haploid UV system and identifies several features of general relevance to the evolution of sex chromosomes.

Highlights

Long-term evolution of sex chromosomes is a dynamic process shaped by gene gain and gene loss
Conservation of sex-determining region gene content among brown algae Sequence analysis of the U and V sex chromosomes of Ectocarpus sp. showed that the male haplotype of the SDR contains 17 protein-coding genes and two pseudogenes, whereas the female haplotype consists of 15 protein-coding genes and seven pseudogenes (Additional file 1: Table S1) [28]
A core set of genes has been maintained in the brown algal SDRs over the last 80–110 million years (MY), both gene gain and gene loss have played an important role in shaping the evolution of these chromosomal regions

Summary

Introduction

Long-term evolution of sex chromosomes is a dynamic process shaped by gene gain and gene loss. Gene loss and gene gain events have been shown to play an important role in the evolution of XY and ZW sex chromosomes in several different metazoan lineages. Species with XY chromosomes have a significant excess of genes moving out of the X chromosome compared with autosomes, and these genes tend to acquire male-biased or male-specific expression, suggesting they play a role in male reproduction [1,2,3,4]. In organisms with female heterogamety (ZW systems), an equivalent process is observed, involving gene relocation out of the Z chromosome to autosomes and the evolution of the sex chromosome that is present in only one sex in heterogametic systems (Y or W) has been shaped by both loss and gain of genes. Dynamic changes in the gene content of plant Y chromosomes, including loss of genes and gain of genes with a role in male reproduction, have been documented [6, 18, 19]

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