Abstract

The de novo emergence of new genes has been well documented through genomic analyses. However, a functional analysis, especially of very young protein-coding genes, is still largely lacking. Here, we identify a set of house mouse-specific protein-coding genes and assess their translation by ribosome profiling and mass spectrometry data. We functionally analyze one of them, Gm13030, which is specifically expressed in females in the oviduct. The interruption of the reading frame affects the transcriptional network in the oviducts at a specific stage of the estrous cycle. This includes the upregulation of Dcpp genes, which are known to stimulate the growth of preimplantation embryos. As a consequence, knockout females have their second litters after shorter times and have a higher infanticide rate. Given that Gm13030 shows no signs of positive selection, our findings support the hypothesis that a de novo evolved gene can directly adopt a function without much sequence adaptation.

Highlights

  • The evolution of new genes through duplication-divergence processes is well understood (Chen et al, 2013; Kaessmann, 2010; Long et al, 2013; Tautz and Domazet-Loso, 2011)

  • We have chosen a gene expressed in the female reproductive system to address the question of the role of de novo gene evolution in this as yet little studied context

  • Given that we find no measurable acceleration of sequence evolution in the gene, we conclude that it became directly functional after its open reading frame became functional

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Summary

Introduction

The evolution of new genes through duplication-divergence processes is well understood (Chen et al, 2013; Kaessmann, 2010; Long et al, 2013; Tautz and Domazet-Loso, 2011). With the increasing availability of comparative genome data from closely related species, more and more cases of unequivocal de novo gene emergence have been described (McLysaght and Hurst, 2016; Schlotterer, 2015; Tautz, 2014; Tautz and Domazet-Loso, 2011). These analyses have shown that de novo gene emergence is a very active process in all evolutionary lineages analyzed. Considering that the mammalian females have complex reproduction cycles, including morphology, physiology and behavior relating to mate choice, pregnancy, and parenting, de novo genes in mammals should be expected to have a function in female-specific organs and affect female fertility and reproductive behavior as well

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