Chromatin profiling identifies transcriptional readthrough as a conserved mechanism for piRNA cluster biogenesis in mosquitoes

Abstract

The piRNA pathway in mosquitoes differs substantially from other model organisms, with an expanded PIWI gene family and functions in antiviral defense. Here, we defined core piRNA clusters as small RNA source loci that showed ubiquitous expression in both somatic and germline tissues. These core piRNA clusters were enriched for non-retroviral endogenous viral elements (nrEVEs) in antisense orientation and depended on key biogenesis factors, Nxf1, Veneno, Tejas, Yb, and Shutdown. Combined transcriptome and chromatin state analyses identified transcriptional readthrough as a conserved mechanism for piRNA cluster biogenesis in Aedes aegypti, Aedes albopictus, Culex quinquefasciatus, and Anopheles gambiae. Comparative analyses between two Aedes mosquitoes suggested that piRNA clusters function as traps for nrEVEs, allowing adaptation to environmental challenges such as virus infection. Our systematic transcriptome and chromatin state analyses lay the foundation for studies of gene regulation, genome evolution and piRNA functions in these important vector species. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=200 SRC="FIGDIR/small/504762v2_ufig1.gif" ALT="Figure 1"> View larger version (55K): org.highwire.dtl.DTLVardef@388aeborg.highwire.dtl.DTLVardef@28640forg.highwire.dtl.DTLVardef@1c12440org.highwire.dtl.DTLVardef@1331e0b_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LICore piRNA clusters showed ubiquitous expression in both somatic and germline tissues in four vector mosquitoes. C_LIO_LIChromatin profiling identifies transcriptional readthrough as a conserved mechanism for piRNA biogenesis. C_LIO_LIBiogenesis of cluster-derived piRNAs depends on key factors, Nxf1, Veneno, Tejas, Yb, and Shutdown. C_LIO_LIpiRNA clusters function as traps for viral elements downstream of conserved set of genes in Aedes mosquitoes C_LI