Stellate Genes and the piRNA Pathway in Speciation and Reproductive Isolation of Drosophila melanogaster.

Vladimir E Adashev,Alexei A Aravin,Sergei S Bazylev,Ludmila V Olenina,Aleksei S Shatskikh,Alexei A Kotov

doi:10.3389/fgene.2020.610665

Vladimir E Adashev, Alexei A Aravin + Show 4 more

Open Access

https://doi.org/10.3389/fgene.2020.610665

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Abstract

One of the main conditions of the species splitting from a common precursor lineage is the prevention of a gene flow between diverging populations. The study of Drosophila interspecific hybrids allows to reconstruct the speciation mechanisms and to identify hybrid incompatibility factors that maintain post-zygotic reproductive isolation between closely related species. The regulation, evolution, and maintenance of the testis-specific Ste-Su(Ste) genetic system in Drosophila melanogaster is the subject of investigation worldwide. X-linked tandem testis-specific Stellate genes encode proteins homologous to the regulatory β-subunit of protein kinase CK2, but they are permanently repressed in wild-type flies by the piRNA pathway via piRNAs originating from the homologous Y-linked Su(Ste) locus. Derepression of Stellate genes caused by Su(Ste) piRNA biogenesis disruption leads to the accumulation of crystalline aggregates in spermatocytes, meiotic defects and male sterility. In this review we summarize current data about the origin, organization, evolution of the Ste-Su(Ste) system, and piRNA-dependent regulation of Stellate expression. The Ste-Su(Ste) system is fixed only in the D. melanogaster genome. According to our hypothesis, the acquisition of the Ste-Su(Ste) system by a part of the ancient fly population appears to be the causative factor of hybrid sterility in crosses of female flies with males that do not carry Y-linked Su(Ste) repeats. To support this scenario, we have directly demonstrated Stellate derepression and the corresponding meiotic disorders in the testes of interspecies hybrids between D. melanogaster and D. mauritiana. This finding embraces our hypothesis about the contribution of the Ste-Su(Ste) system and the piRNA pathway to the emergence of reproductive isolation of D. melanogaster lineage from initial species.

Highlights

At the beginning of the XXI century, a new class of small regulatory RNAs, piRNAs, was discovered in the testes of Drosophila melanogaster (Aravin et al, 2001, 2004; Vagin et al, 2006)
Analysis of recent genome assemblies of the simulans clade species reveals that pseudo-βCK2tes repeat (PCKR) duplications are present in the Y chromosome of all three sibling species, D. simulans, D. mauritiana, and D. sechellia, in the range from 22 to 117 copies (Chakraborty et al, 2020)
We revealed that vasa sequences from closely related species, D. simulans, D. sechellia and D. mauritiana, that have diverged from an ancestor common with D. melanogaster 2.0–5.4 million years ago (Russo et al, 1995; Tamura et al, 2004), maintain more than 90% complementarity with piRNAs from AT-chX repeats of D. melanogaster compared with only 76% for vasa of D. melanogaster itself (Kotov et al, 2019)

Summary

INTRODUCTION

At the beginning of the XXI century, a new class of small regulatory RNAs, piRNAs, was discovered in the testes of Drosophila melanogaster (Aravin et al, 2001, 2004; Vagin et al, 2006). Euchromatic Stellate genes carry a 16 bp deletion in the corresponding region of the promoter, which could be a sign of the insertion and subsequent imperfect excision of hoppel (Olenkina et al, 2012a) This data argues for the hypothesis according to which ancestral copies of euchromatic and heterochromatic Stellate clusters translocate on the X chromosome independently and at different stages of the evolutionary history of the Ste-Su(Ste) family. Analysis of recent genome assemblies of the simulans clade species reveals that pseudo-βCK2tes repeat (PCKR) duplications are present in the Y chromosome of all three sibling species, D. simulans, D. mauritiana, and D. sechellia, in the range from 22 to 117 copies (Chakraborty et al, 2020) These findings allow suggesting that the first stages of the Ste-Su(Ste) system formation occurred before the splitting of D. melanogaster from the common precursor, but subsequent dynamics of the evolution process led to species diversification. The functional significance of these possible interactions is unexplored to date

MELANOGASTER

MELANOGASTER AND CLOSELY

Findings

CONCLUSIONS AND PERSPECTIVES