A teratocyte‐specific serpin from the endoparasitoid wasp Cotesia vestalis inhibits the prophenoloxidase‐activating system of its host Plutella xylostella

Abstract

Many endoparasitoids adopt several parasitic factors, such as venom, polydnavirus and teratocytes, to suppress the immune response of their associated hosts including melanization for successful parasitism. A teratocyte-specific expressed serpin gene, designated as CvT-serpin6, was identified from the parasitoid Cotesia vestalis. The immunoblot result suggested that CvT-serpin6 was secreted into extracellular space. qPCR results showed that CvT-serpin6 was mainly transcribed at later stages of parasitism, and the transcriptional abundance of CvT-serpin6 in teratocytes was significantly increased in response to the challenge of bacteria. Inhibitory assay indicated that recombinant CvT-serpin6 (rCvT-serpin6) could inhibit the activation of Plutella xylostella prophenoloxidase and ultimately resulted in the inhibition of melanization in P. xylostella haemolymph.Furthermore, we confirmed that rCvT-serpin6 could form SDS-stable complexes with activated PxPAP1 and PxPAP3 in a dose-dependent manner. Altogether, our results further shed insight into the molecular mechanisms that teratocytes involved in controlling host immune response.

Parasitoid Serpins Evolve Novel Functions to Manipulate Host Homeostasis

“…1B ). Interestingly, apart from the 2 characterized serpins ( Gu et al 2021 , 2022 ), 8 additional serpins are teratocyte-specific with high expression and thus were named “ C. vestalis teratocyte serpins ( CvT-serpins )”.…”

“…Further positive selection analysis showed that the residue around the P1–P1′ cleavage sites of the RCL was under significantly positive selection. Notably, in addition to the 2 characterized serpins ( Gu et al 2021 , 2022 ), 8 more serpins are teratocyte-specific and highly expressed, which leads us to ask whether the functions of these serpins are conserved and how the biological importance of serpins is represented in the parasitic lifestyle of C. vestalis . Our results showed that all these serpins show inhibitory activities and play multiple physiological roles in the host-parasitoid system.…”

A parasitoid serpin gene that disrupts host immunity shows adaptive evolution of alternative splicing

“…To manipulate their hosts, parasitoid wasps often recruit effector genes, e.g., venom or larval salivary genes 14,15 . Serpin, a common component of parasitoid venom 17, 20–23, 33–41 , has also been reported in teratocytes of parasitoid wasps for host regulation 53,54 . Here, we further extend serpin recruitment to wasp larval saliva.…”

“…The copyright holder for this preprint this version posted March 29, 2023. ; https://doi.org/10.1101/2023.03.28.534536 doi: bioRxiv preprint larval salivary genes 14,15 . Serpin, a common component of parasitoid venom 17,[20][21][22][23][33][34][35][36][37][38][39][40][41] , has also been reported in teratocytes of parasitoid wasps for host regulation 53,54 . Here, we further extend serpin recruitment to wasp larval saliva.…”

Pleiotropic immunoregulation by growth‐blocking peptide in Ostrinia furnacalis

“…These pathways regulate AMP expression through transcription factors in the rel family, such as Dorsal/Dif and Relish (Asgari et al, 2022; Nishide et al, 2019; Palmer et al, 2018). Phenoloxidase (PO)‐catalysed melanization is a vital mechanism in insects and crustaceans (Gu et al, 2022; Marieshwari et al, 2023), which generates 5,6‐dihydroxyindole for oxidation and polymerisation into melanin deposited on the surface of pathogens to kill and immobilise them (Nakhleh et al, 2017 ).…”