What Are the Functional Roles of Piwi Proteins and piRNAs in Insects?

SIMPLE SUMMARY: Three small RNA pathways, representing miRNAs, siRNAs and piRNAs, exist in insects. Of the three pathways, piRNAs and Piwi proteins appear to have the most complex biogenesis and functional roles. Significant progress has recently occurred in the understanding of the piRNA pathway in three major research areas, i.e., oogenesis and spermatogenesis in the fruitfly, antiviral response in mosquitoes and piRNA biogenesis in silkworm-derived BmN4 cells. Thus, it is timely to provide an overview of the knowledge accumulated so far. Studies in other insects are lagging behind but are highly anticipated since piRNAs and Piwi proteins are abundantly expressed not only in the germline but also in the somatic tissues. Due to the diversification of Piwi genes among insects, novel functions of piRNAs and Piwi proteins can be expected in the different species. This comprehensive review aimed to provide important background information about the current knowledge on piRNAs and Piwi proteins in insects that can function as a resource for future research. ABSTRACT: Research on Piwi proteins and piRNAs in insects has focused on three experimental models: oogenesis and spermatogenesis in Drosophila melanogaster, the antiviral response in Aedes mosquitoes and the molecular analysis of primary and secondary piRNA biogenesis in Bombyx mori-derived BmN4 cells. Significant unique and complementary information has been acquired and has led to a greater appreciation of the complexity of piRNA biogenesis and Piwi protein function. Studies performed in other insect species are emerging and promise to add to the current state of the art on the roles of piRNAs and Piwi proteins. Although the primary role of the piRNA pathway is genome defense against transposons, particularly in the germline, recent findings also indicate an expansion of its functions. In this review, an extensive overview is presented of the knowledge of the piRNA pathway that so far has accumulated in insects. Following a presentation of the three major models, data from other insects were also discussed. Finally, the mechanisms for the expansion of the function of the piRNA pathway from transposon control to gene regulation were considered.