Pseudogerm of the parasitoid Macrocentrus cingulum suppresses host pupation by degenerating prothoracic gland and inhibiting the expression of Br-C in the host Ostrinia furnacalis.

Background: Parasitic wasps manipulate host development for successful parasitization. When the host Ostrinia furnacalis is parasitized by the parasitoid Macrocentrus cingulum, its larvae fail to pupate and are consumed as nutrition by the wasp larvae. However, the mechanism by which M. cingulum modulates host pupation remains unclear. This study reports on pseudogerm, a newly discovered parasitic factor derived from M. cingulum, which plays a regulatory role in the pupation process of the host.

Results: Ostrinia furnacalis larvae transplanted with pseudogerms failed to pupate, and their prothoracic gland (PG) cells did not enlarge significantly at the prepupal stage compared to the control. Additionally, the nuclei of PG cells fragmented, the number of secretory vesicles in the cytoplasm decreased markedly, and the intracellular channel system on the cell membrane atrophied. Furthermore, the elevation of the 20-hydroxyecdysone (20E) titer at the prepupal stage was also suppressed, indicating that pseudogerm disrupts the ecdysteroid level by causing PG cell degeneration. Additionally, there was a suppression of Broad Complex (Br-C) expression in O. furnacalis larvae before the prepupal stage due to pseudogerms transplantation. When OfBr-C was knocked down by RNA-interference or knocked out by CRISPR/Cas9, approximately 24% and 48.3% of O. furnacalis larvae failed to pupate, respectively.

Conclusion: Pseudogerm potentially disrupts the 20E titer by destroying the host's PG and further inhibits the expression of OfBr-C, ultimately preventing host pupation. This study provides new insights into the strategies employed by parasitoids in controlling host development. © 2024 Society of Chemical Industry.