Regulation of melanization in aphids by parasitoid wasp venom proteins enhances mummification

Abstract Background Interactions between parasitic insects and their hosts demonstrate the complexity of evolutionary processes. Specifically, the parasitoid wasp Aphidius ervi manipulates its host, the pea aphid Acyrthosiphon pisum , through strategic venom injection to enhance mummification. This study explores how this venom affects the aphid's immune system, particularly targeting the activity of the phenoloxidase (PO) enzyme. Results Following the injection of venom from A . ervi , significant changes were observed in the expression of immune‐related genes in A . pisum , especially notable expression changes of ApPPO s and a reduction of PO activity. Multi‐omics sequencing identified 74 potential venom proteins in the venom gland of A . ervi , including serine protease homolog 1 (AeSPH1) and serine protease inhibitor (AeSPN1), hypothesized to regulate PO activity. The injection of recombinant protein AeSPH1 and AeSPN1 into the A . pisum hemocoel selectively reduced the expression of ApPPO1 , without affecting ApPPO2 , and effectively suppressed melanization. Moreover, RNAi targeting AeSPH1 significantly reduced the mummification rate in A . pisum population parasitized by A . ervi . Conclusion Our findings clarify the complex biochemical mechanisms underlying host‐wasp interactions and highlight potential avenues for developing targeted biological control strategies. © 2024 Society of Chemical Industry.