Sex chromosome dominance in a UV sexual system

Abstract

The alternation between multicellular haploid gametophytes and diploid sporophytes is a defining feature of most plant and algal life cycles. In such organisms, male and female sexes are determined in the haploid gametophyte with a female (U) or male (V) sex chromosome. Once the U and V chromosomes unite at fertilisation, sex determination no longer occurs, raising key questions about the fate of UV sex chromosomes in the diploid sporophyte stage of the life cycle. Here, we unravel the genetic and molecular interactions between the U and V chromosomes by assessing transcriptional and chromatin states across the life cycle of the brown alga Ectocarpus alongside ouroboros mutants that decouple life cycle stage from ploidy. We reveal how sex chromosome genes are developmentally regulated across the life cycle, with genes involved in female sex determination in particular undergoing strong down-regulation in the sporophyte. Diploid ouroboros mutants containing both a U and V sex chromosome behave as functional male gametophytes yet still exhibit feminized transcription, suggesting that presence of the V chromosome alone is insufficient to fully suppress female developmental program. Although the silencing of sex chromosome genes in the diploid sporophyte does not appear to correlate with localised changes in chromatin state, small RNAs may play a role in the repression of a female sex-linked gene. Finally, we show how histone H3K79me2 is globally re-configured in the diploid phase of the life cycle, including the sex determining region of the UV sex chromosomes. Contrary to its pattern in the haploid gametophyte, H3K79me2 no longer associates with repressed genes in the diploid sporophyte, suggesting that the function of this histone mark in Ectocarpus may be more complex than previously appreciated.