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Adaptive evolution among cytoplasmic piRNA proteins leads to decreased genomic auto-immunity.

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.

SUBMITTER: Wang L

PROVIDER: S-EPMC7310878 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Adaptive evolution among cytoplasmic piRNA proteins leads to decreased genomic auto-immunity.

Wang Luyang L Barbash Daniel A DA Kelleher Erin S ES

PLoS genetics 20200611 6

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 sequence ...[more]

PMID: 32525870

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Project description:BackgroundDetection of adaptive amino acid changes in proteins under recent short-term selection is of great interest for researchers studying microevolutionary processes in microbial pathogens or any other biological species. However, independent occurrence of such point mutations within genetically diverse haplotypes makes it difficult to detect the selection footprint by using traditional molecular evolutionary analyses. The recently developed Zonal Phylogeny (ZP) has been shown to be a useful analytic tool for identifying the footprints of short-term positive selection. ZP separates protein-encoding genes into evolutionarily long-term (with silent diversity) and short-term (without silent diversity) categories, or zones, followed by statistical analysis to detect signs of positive selection in the short-term zone. However, successful broad application of ZP for analysis of large haplotype datasets requires automation of the relatively labor-intensive computational process.ResultsHere we present Zonal Phylogeny Software (ZPS), an application that describes the distribution of single nucleotide polymorphisms (SNPs) of synonymous (silent) and non-synonymous (replacement) nature along branches of the DNA tree for any given protein-coding gene locus. Based on this information, ZPS separates the protein variant haplotypes with silent variability (Primary zone) from those that have recently evolved from the Primary zone variants by amino acid changes (External zone). Further comparative analysis of mutational hot-spot frequencies and haplotype diversity between the two zones allows determination of whether the External zone haplotypes emerged under positive selection.ConclusionsAs a visualization tool, ZPS depicts the protein tree in a DNA tree, indicating the most parsimonious numbers of synonymous and non-synonymous changes along the branches of a maximum-likelihood based DNA tree, along with information on homoplasy, reversion and structural mutation hot-spots. Through zonal differentiation, ZPS allows detection of recent adaptive evolution via selection of advantageous structural mutations, even when the advantage conferred by such mutations is relatively short-term (as in the case of "source-sink" evolutionary dynamics, which may represent a major mode of virulence evolution in microbes).

Dataset Information

Adaptive evolution among cytoplasmic piRNA proteins leads to decreased genomic auto-immunity.

Publications

Adaptive evolution among cytoplasmic piRNA proteins leads to decreased genomic auto-immunity.

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