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

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

JOURNAL=Frontiers in Genetics

VOLUME=11

YEAR=2021

URL=https://www.frontiersin.org/journals/genetics/articles/10.3389/fgene.2020.610665

DOI=10.3389/fgene.2020.610665

ISSN=1664-8021

ABSTRACT=<p>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 <italic>Drosophila</italic> 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 <italic>Ste-Su(Ste)</italic> genetic system in <italic>Drosophila melanogaster</italic> is the subject of investigation worldwide. X-linked tandem testis-specific <italic>Stellate</italic> 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 <italic>Su(Ste)</italic> locus. Derepression of <italic>Stellate</italic> genes caused by <italic>Su(Ste)</italic> 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 <italic>Ste-Su(Ste)</italic> system, and piRNA-dependent regulation of <italic>Stellate</italic> expression. The <italic>Ste-Su(Ste)</italic> system is fixed only in the <italic>D. melanogaster</italic> genome. According to our hypothesis, the acquisition of the <italic>Ste-Su(Ste)</italic> 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 <italic>Su(Ste)</italic> repeats. To support this scenario, we have directly demonstrated <italic>Stellate</italic> derepression and the corresponding meiotic disorders in the testes of interspecies hybrids between <italic>D. melanogaster</italic> and <italic>D. mauritiana</italic>. This finding embraces our hypothesis about the contribution of the <italic>Ste-Su(Ste)</italic> system and the piRNA pathway to the emergence of reproductive isolation of <italic>D. melanogaster</italic> lineage from initial species.</p>