Regulation of the X Chromosome in the Germline and Soma of Drosophila melanogaster Males

Eliza Argyridou,John Parsch

doi:10.3390/genes9050242

Abstract

During the evolution of heteromorphic sex chromosomes, the sex-specific Y chromosome degenerates, while the X chromosome evolves new mechanisms of regulation. Using bioinformatic and experimental approaches, we investigate the expression of the X chromosome in Drosophila melanogaster. We observe nearly complete X chromosome dosage compensation in male somatic tissues, but not in testis. The X chromosome contains disproportionately fewer genes with high expression in testis than the autosomes, even after accounting for the lack of dosage compensation, which suggests that another mechanism suppresses their expression in the male germline. This is consistent with studies of reporter genes and transposed genes, which find that the same gene has higher expression when autosomal than when X-linked. Using a new reporter gene that is expressed in both testis and somatic tissues, we find that the suppression of X-linked gene expression is limited to genes with high expression in testis and that the extent of the suppression is positively correlated with expression level.

Highlights

In many animal species with a long evolutionary history of having separate sexes, heteromorphic sex chromosomes are thought to have evolved when an ancestral pair of autosomes gained a sex-determining locus [1,2]
We find evidence for nearly complete X chromosome dosage compensation in somatic tissues, genes with very high expression are underrepresented on the X chromosome
We found that the expression of X-linked genes was significantly lower than autosomal genes (Table 1), with the median expression of X-linked genes being 65% that of autosomal genes

Summary

Introduction

In many animal species with a long evolutionary history of having separate sexes, heteromorphic sex chromosomes are thought to have evolved when an ancestral pair of autosomes gained a sex-determining locus [1,2]. During this early stage of sex chromosome evolution, the accumulation of sexually antagonistic mutations (mutations that are beneficial to one sex but detrimental to the other) in the region surrounding the sex-determining locus provides selective pressure to inhibit recombination between the homologous chromosomes, as it would be deleterious for such mutations to be expressed in the wrong sex.

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Conclusion