Multiple gene movements into and out of haploid sex chromosomes

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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-017-1201-7) contains supplementary material, which is available to authorized users.

Isolation and expression analysis of a candidate gametophyte sex determination gene (sjhmg) of kelp (Saccharina japonica)

“…This result was consistent with the findings in the conservative analysis of SDR genes among brown algae by Lipinska et al. (). The prediction of protein domains revealed that SjHMG has two typical HMG‐box domains.…”

“…( Ec‐13_001750 ), which implied that it was a candidate sex‐determining gene (Lipinska et al. ). In this study, the male‐specific SjHMG gene was found to be orthologous to the male SDR gene Ec‐13_001750 of Ectocarpus , which was conservative among other brown algae with the UV sex determination system (Lipinska et al.…”

“…, Lipinska et al. ). As was predicted, the gene encodes a member of the HMG domain‐containing proteins, which play a key role in sex determination in several animal and fungal species (Gubbay et al.…”

“…In addition, this gene is the only gene that is limited to the male SDR across seven other brown algal species (Lipinska et al. ). Therefore, there is accumulating evidence that the orthologous gene of Ec‐13_001750 in S. japonica may also function as the sex determiner of S. japonica gametophytes.…”

Parthenogenesis is rare in the reproduction of a sexual field population of the isogamous brown alga Scytosiphon (Scytosiphonaceae, Ectocarpales)

“…Partial sequences of the sex‐specific non‐recombining regions in the female and male sex‐determining regions (Lipinska et al. ) were amplified and used as the sex markers (Hoshino et al. 2018b).…”