Rapid Evolution of piRNA Pathway in the Teleost Fish: Implication for an Adaptation to Transposon Diversity

Abstract

The Piwi-interacting RNA (piRNA) pathway is responsible for germline specification, gametogenesis, transposon silencing, and genome integrity. Transposable elements can disrupt genome and its functions. However, piRNA pathway evolution and its adaptation to transposon diversity in the teleost fish remain unknown. This article unveils evolutionary scene of piRNA pathway and its association with diverse transposons by systematically comparative analysis on diverse teleost fish genomes. Selective pressure analysis on piRNA pathway and miRNA/siRNA (microRNA/small interfering RNA) pathway genes between teleosts and mammals showed an accelerated evolution of piRNA pathway genes in the teleost lineages, and positive selection on functional PAZ (Piwi/Ago/Zwille) and Tudor domains involved in the Piwi–piRNA/Tudor interaction, suggesting that the amino acid substitutions are adaptive to their functions in piRNA pathway in the teleost fish species. Notably five piRNA pathway genes evolved faster in the swamp eel, a kind of protogynous hermaphrodite fish, than the other teleosts, indicating a differential evolution of piRNA pathway between the swamp eel and other gonochoristic fishes. In addition, genome-wide analysis showed higher diversity of transposons in the teleost fish species compared with mammals. Our results suggest that rapidly evolved piRNA pathway in the teleost fish is likely to be involved in the adaption to transposon diversity.

Adaptive Evolution Leads to Cross-Species Incompatibility in the piRNA Transposon Silencing Machinery

“…The piRNA pathway has a conserved function in germline development and transposon silencing, but piRNA sequence composition and biogenesis mechanisms show remarkable phylogenetic diversity, and many genes in the piRNA pathway are evolving rapidly under positive selection, and are poorly conserved (Chirn et al, 2015; Khurana and Theurkauf, 2010; Obbard et al, 2009; Simkin et al, 2013; Yi et al, 2014; Zanni et al, 2013). We directly determined the functional consequences of piRNA gene divergence over a short evolutionary time scale, by expressing the simulans rhi and del genes in melanogaster and assaying protein interactions, subcellular localization, and the ability to rescue chromosomal mutations.…”

“…Mutations that disrupt the piRNA pathway lead to sterility and transposon mobilization in worms, flies, fish and mice, and have been linked to human infertility (Batista et al, 2008; Carmell et al, 2007; Das et al, 2008; Gou et al, 2017; Gu et al, 2010; Heyn et al, 2012; Houwing et al, 2008; Lin and Spradling, 1997; Weick and Miska, 2014). In striking contrast, genes with essential functions in piRNA production and transposon silencing in established model systems are often very poorly conserved, and piRNA biogenesis and sequence composition show remarkable phylogenetic diversity (Chirn et al, 2015; Obbard et al, 2009; Simkin et al, 2013; Yi et al, 2014; Zanni et al, 2013). For example , the overwhelming majority of piRNAs in the Drosophila female germline map to transposons and are derived from heterochromatic domains that span hundreds of kilobases.…”

Host–transposon interactions: conflict, cooperation, and cooption

“…Signatures of positive selection are pervasive in invertebrate piRNA pathway proteins, operating at virtually every step of piRNA biogenesis both within and between species (Begun et al 2007;Larracuente et al 2008;Obbard et al 2009;Mackay et al 2012;Simkin et al 2013;Blumenstiel et al 2016). Signatures of positive selection are also apparent in the evolution of several piRNA genes across fish species, including Piwil1, but less evident in their mammalian homologs (Yi et al 2014).…”

Transposons, Genome Size, and Evolutionary Insights in Animals

“…This mechanism, which in some cases may be influenced by sRNAs [Wheeler, 2013;Yi et al, 2014], appears to be less generalized, especially in animals. Indeed, repeated elements are generally highly methylated in plants, yeast, and vertebrates but are less methylated in protostomes, especially in insects [Albalat et al, 2012].…”