Abstract
Evolutionarily young genes are usually preferentially expressed in the testis across species. Although it is known that older genes are generally more broadly expressed than younger genes, the properties that shaped this pattern are unknown. Older genes may gain expression across other tissues uniformly, or faster in certain tissues than others. Using Drosophila gene expression data, we confirmed previous findings that younger genes are disproportionately testis biased and older genes are disproportionately ovary biased. We found that the relationship between gene age and expression is stronger in the ovary than any other tissue and weakest in testis. We performed ATAC-seq on Drosophila testis and found that although genes of all ages are more likely to have open promoter chromatin in testis than in ovary, promoter chromatin alone does not explain the ovary bias of older genes. Instead, we found that upstream transcription factor (TF) expression is highly predictive of gene expression in ovary but not in testis. In the ovary, TF expression is more predictive of gene expression than open promoter chromatin, whereas testis gene expression is similarly influenced by both TF expression and open promoter chromatin. We propose that the testis is uniquely able to express younger genes controlled by relatively few TFs, whereas older genes with more TF partners are broadly expressed with peak expression most likely in the ovary. The testis allows widespread baseline expression that is relatively unresponsive to regulatory changes, whereas the ovary transcriptome is more responsive to trans-regulation and has a higher ceiling for gene expression.
Highlights
Genes have continuously arisen by a multitude of ways, from duplication and divergence to de novo origination from non-genic DNA (Begun et al, 2006; Long et al, 2003; Ohno, 1970; Tautz and Domazet-Lošo, 2011; Zhao et al, 2014; Zhou et al, 2008)
We found that ovarybiased genes tend to have higher upstream transcription factor (TF) expression than testis-biased genes of all age groups, yet young genes, with fewer TF partners, tend to be testis-expressed and old genes, with more TF partners, tend to be ovary biased
Whereas young genes are often testis-biased and highly tissue specific, old genes are broadly expressed with peak expression in ovary
Summary
Genes have continuously arisen by a multitude of ways, from duplication and divergence to de novo origination from non-genic DNA (Begun et al, 2006; Long et al, 2003; Ohno, 1970; Tautz and Domazet-Lošo, 2011; Zhao et al, 2014; Zhou et al, 2008). A large portion of young genes segregate within or recently fixed in populations, and most young genes are expressed in the testis (Levine et al, 2006; Zhao et al, 2014), similar to duplicated genes (Long et al, 2013). The phrase “out of the testis” was originally used to describe young retroposed genes (Vinckenbosch et al, 2006), which gained expression by exploiting cis-regulatory machinery of nearby genes. Testis-bias has since been observed in young X-linked duplicate genes, leading researchers to propose that young genes escape Meiotic Sex Chromosome Inactivation (MSCI) due to immature cis-regulatory machinery (Zhang et al, 2010a). Testis expresses more genes in general than any other tissue (Soumillon et al, 2013), and studies from many taxa support that a large proportion of young genes to show testis-biased or testis-specific expression and function (see review in Long et al, 2013)
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