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Adaptive evolution among cytoplasmic piRNA proteins leads to decreased genomic auto-immunity.
- Source :
-
PLoS genetics [PLoS Genet] 2020 Jun 11; Vol. 16 (6), pp. e1008861. Date of Electronic Publication: 2020 Jun 11 (Print Publication: 2020). - Publication Year :
- 2020
-
Abstract
- In metazoan germlines, the piRNA pathway acts as a genomic immune system, employing small RNA-mediated silencing to defend host DNA from the harmful effects of transposable elements (TEs). Expression of genomic TEs is proposed to initiate self regulation by increasing the production of repressive piRNAs, thereby "adapting" piRNA-mediated control to the most active TE families. Surprisingly, however, piRNA pathway proteins, which execute piRNA biogenesis and enforce silencing of targeted sequences, evolve rapidly and adaptively in animals. If TE silencing is ensured through piRNA biogenesis, what necessitates changes in piRNA pathway proteins? Here we used interspecific complementation to test for functional differences between Drosophila melanogaster and D. simulans alleles of three adaptively evolving piRNA pathway proteins: Armitage, Aubergine and Spindle-E. In contrast to piRNA-mediated transcriptional regulators examined in previous studies, these three proteins have cytoplasmic functions in piRNA maturation and post-transcriptional silencing. Across all three proteins we observed interspecific divergence in the regulation of only a handful of TE families, which were more robustly silenced by the heterospecific piRNA pathway protein. This unexpected result suggests that unlike transcriptional regulators, positive selection has not acted on cytoplasmic piRNA effector proteins to enhance their function in TE repression. Rather, TEs may evolve to "escape" silencing by host proteins. We further discovered that D. simulans alleles of aub and armi exhibit enhanced off-target effects on host transcripts in a D. melanogaster background, as well as modest reductions in the efficiency of piRNA biogenesis, suggesting that promiscuous binding of D. simulans Aub and Armi proteins to host transcripts reduces their participation in piRNA production. Avoidance of genomic auto-immunity may therefore be a critical target of selection. Our observations suggest that piRNA effector proteins are subject to an evolutionary trade-off between defending the host genome from the harmful effect of TEs while also minimizing collateral damage to host genes.<br />Competing Interests: The authors have declared that no competing interests exist.
- Subjects :
- Alleles
Animals
Animals, Genetically Modified
Cytoplasm genetics
Cytoplasm metabolism
DNA Transposable Elements genetics
Drosophila Proteins genetics
Drosophila Proteins immunology
Drosophila Proteins metabolism
Drosophila melanogaster genetics
Drosophila melanogaster immunology
Drosophila melanogaster metabolism
Drosophila simulans metabolism
Female
Gene Expression Regulation immunology
Genome, Insect genetics
Male
Mutation
RNA Interference immunology
Autoimmunity genetics
DNA Transposable Elements immunology
Drosophila simulans genetics
Evolution, Molecular
Genome, Insect immunology
RNA, Small Interfering biosynthesis
Subjects
Details
- Language :
- English
- ISSN :
- 1553-7404
- Volume :
- 16
- Issue :
- 6
- Database :
- MEDLINE
- Journal :
- PLoS genetics
- Publication Type :
- Academic Journal
- Accession number :
- 32525870
- Full Text :
- https://doi.org/10.1371/journal.pgen.1008861