BdPiwi is essential for gametogenesis and post-embryonic development in the oriental fruit fly, Bactrocera dorsalis

The PIWI-interacting RNA (piRNA) pathway is a conserved transposon silencing mechanism essential for genomic integrity and gametogenesis. While Piwi proteins are known to play essential roles in insect germline development, their functional characteristics remain largely unexplored in agricultural pests. Here, we investigated BdPiwi in Bactrocera dorsalis, a highly invasive pest whose exceptional reproductive capacity underpins its global pest status.

Phylogenetic analysis revealed that BdPiwi is evolutionarily conserved among insects and contains the canonical PAZ and PIWI domains. Spatiotemporal profiling showed ubiquitous expression across developmental stages, with predominant enrichment in adult ovaries. Based on CRISPR/Cas9-mediated mutagenesis, we found that BdPiwi loss caused severe gonadal arrest and complete sterility in both sexes-females lacked detectable oocytes and males produced no mature sperm. Transcriptomic analysis uncovered widespread transcriptional upregulation, extensive transposon derepression, and dysregulated immunometabolic genes likely contributing to oogenic failure. Additionally, mutants exhibited prolonged larval duration and abnormal eclosion.

These findings demonstrate that BdPiwi is a pleiotropic regulator governing gonadogenesis, fertility, and metamorphic transition in B. dorsalis. This study expands the functional repertoire of Piwi genes in insect pests and provides a promising molecular target for genetic-based management of this devastating invasive species. © 2026 Society of Chemical Industry.