trans-homolog interaction regulates the sex-biased expression of an X-linked gene

Abstract

Sex-biased gene expression patterns in animals are generally controlled by the somatic sex-determination hierarchies. How the different tiers of these hierarchies act on sexually dimorphic gene regulation is still poorly understood. In the developing Drosophila biarmipes wing, the X-linked gene yellow is expressed in males in a specific distal spot pattern that prefigures a corresponding adult pigmentation pattern. This yellow expression pattern is controlled by the spot enhancer, but the origin of yellow sexually dimorphic expression is unknown. Here we find that the functional interaction between homologous yellow alleles silences specifically the spot enhancer, which is therefore active in males (XY) but not in females (XX). We show that inserting yellow at homologous positions on autosomes recapitulates, in either sex, the homologousdependent silencing of the spot enhancer. We further find that this silencing requires the yellow intron as well as the architectural protein Mod(mdg4). Finally, we show that Mod(mdg4) is also necessary for the sex-biased expression of some X-linked genes in the brain. Our results demonstrate that regulatory interactions between X-linked homologous alleles promote their sex-biased expression, independently of the canonical sex-determination hierarchy. More generally, they illustrate the biological significance of homologous chromosome pairing and trans-homolog interactions for the sexually dimorphic regulation of X-linked genes.Sexual dimorphism in morphology, physiology and behaviour is pervasive in animals. Sexbiased gene expression patterns, deployed during embryonic or adult development, direct the formation of these phenotypic sex-specific differences 1 . It is well established that the transcriptional regulators of the somatic sex-determination hierarchies directly control sexually dimorphic gene regulation 1-3 . Yet, the different tiers of these hierarchies seem to contribute to this control through a variety of regulatory mechanisms 1-7 . To better understand the molecular mechanisms governing sexually dimorphic gene regulation, we examined the dimorphic regulation of the yellow (y) gene in D. biarmipes, a species that has evolved a male-specific wing pigmentation spot ( Fig. 1a) 8,9 . During late pupal wing development in D.biarmipes males, Yellow spatial distribution prefigures the adult pigmentation spot (Fig. 1b).In females, only a handful of cells produce Yellow, forming a typical dotted, stochastic pattern (Fig. 1d). Accordingly, almost no pigmentation pattern appears in adult females (Fig. 1c). We first examined the contribution of the top tier of the somatic sex-determination hierarchy, which initiates and establishes female identity in a cell-autonomous manner in

Widespread misregulation of inter-species hybrid transcriptomes due to sex-specific and sex-chromosome regulatory evolution

“…Genes that show cis -only divergence on autosomes for male expression often have C. briggsae or C. nigoni dominant expression in hybrids whereas, in females, they are more typically overdominantly expressed ( Fig 4 ). We can think of four potential mechanisms that might contribute to this sex difference and to the cis -dominant effect in general: (1) more extensive post-transcriptional regulation in females [65] might limit transcript abundance through epistatic interactions; (2) greater degradation or turnover of cis -acting binding sites for male-expressed genes [55, 56] could reduce affinity in transcription factor binding activity; (3) the presence of species-specific trans regulators that originate from lineage-specific gene duplication and/or loss resulting in allele-specific trans -regulation; and (4) some form of transvection that causes single-allele expression in hybrids and one of the parent species; this has been identified as a source for the expression of a dimorphic trait in Drosophila [66].…”