The piRNA pathway is an adaptive mechanism that maintains genome stability by repression of selfish genomic elements. In the male germline of
Drosophila melanogaster
repression of
Stellate
genes by piRNAs generated from
Supressor of Stellate
(
Su(Ste)
) locus is required for male fertility, but both
Su(Ste)
piRNAs and their targets are absent in other
Drosophila
species. We found that
D. melanogaster
genome contains multiple X-linked non-coding genomic repeats that have sequence similarity to the protein-coding host gene
vasa
. In the male germline, these
vasa
-related
AT-chX
repeats produce abundant piRNAs that are antisense to
vasa
; however,
vasa
mRNA escapes silencing due to imperfect complementarity to
AT-chX
piRNAs. Unexpectedly, we discovered
AT-chX
piRNAs target
vasa
of
Drosophila mauritiana
in the testes of interspecies hybrids. In the majority of hybrid flies, the testes were strongly reduced in size and germline content. A minority of hybrids maintained wild-type array of premeiotic germ cells in the testes, but in them harmful
Stellate
genes were derepressed due to the absence of
Su(Ste)
piRNAs, and meiotic failures were observed. Thus, the piRNA pathway contributes to reproductive isolation between
D. melanogaster
and closely related species, causing hybrid male sterility via misregulation of two different host protein factors.
Since their discovery more than 60 years ago, satellite repeats are still one of the most enigmatic parts of eukaryotic genomes. Being non-coding DNA, satellites were earlier considered to be non-functional "junk," but recently this concept has been extensively revised. Satellite DNA contributes to the essential processes of formation of crucial chromosome structures, heterochromatin establishment, dosage compensation, reproductive isolation, genome stability and development. Genomic abundance of satellites is under stabilizing selection owing of their role in the maintenance of vital regions of the genome-centromeres, pericentromeric regions, and telomeres. Many satellites are transcribed with the generation of long or small non-coding RNAs. Misregulation of their expression is found to lead to various defects in the maintenance of genomic architecture, chromosome segregation and gametogenesis. This review summarizes our current knowledge concerning satellite functions, the mechanisms of regulation and evolution of satellites, focusing on recent findings in Drosophila. We discuss here experimental and bioinformatics data obtained in Drosophila in recent years, suggesting relevance of our analysis to a wide range of eukaryotic organisms.
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.
The Y chromosome is one of the sex chromosomes found in males of animals of different taxa, including insects and mammals. Among all chromosomes, the Y chromosome is characterized by a unique chromatin landscape undergoing dynamic evolutionary change. Being entirely heterochromatic, the Y chromosome as a rule preserves few functional genes, but is enriched in tandem repeats and transposons. Due to difficulties in the assembly of the highly repetitive Y chromosome sequence, deep analyses of Y chromosome evolution, structure, and functions are limited to a few species, one of them being Drosophila melanogaster. Despite Y chromosomes exhibiting high structural divergence between even closely related species, Y-linked genes have evolved convergently and are mainly associated with spermatogenesis-related activities. This indicates that male-specific selection is a dominant force shaping evolution of Y chromosomes across species. This review presents our analysis of current knowledge concerning Y chromosome functions, focusing on recent findings in Drosophila. Here we dissect the experimental and bioinformatics data about the Y chromosome accumulated to date in Drosophila species, providing comparative analysis with mammals, and discussing the relevance of our analysis to a wide range of eukaryotic organisms, including humans.
Being a conservative marker of germ cells across metazoan species, DEAD box RNA helicase Vasa (DDX4) remains the subject of worldwide investigations thanks to its multiple functional manifestations. Vasa takes part in the preformation of primordial germ cells in a group of organisms and contributes to the maintenance of germline stem cells. Vasa is an essential player in the piRNA-mediated silencing of harmful genomic elements and in the translational regulation of selected mRNAs. Vasa is the top hierarchical protein of germ granules, liquid droplet organelles that compartmentalize RNA processing factors. Here, we survey current advances and problems in the understanding of the multifaceted functions of Vasa proteins in the gametogenesis of different eukaryotic organisms, from nematodes to humans.
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