Immune tolerance of vector beetle to its partner plant parasitic nematode modulated by its insect parasitic nematode

ABSTRACT Immune response of insect vectors to transmitted pathogens or insect hosts against parasites are well studied, whereas the mechanism of tripartite interactions remains elusive. In this study, we investigated the immune interactions of the vector beetle Monochamus alternatus (Ma) to the devastating plant parasitic nematode Bursaphelenchus xylophilus (Bx) and the insect parasitic nematode Howardula phyllotretae (Hp). We report the unique immune mechanism by which the vectorbeetle tolerates many devastating Bx in its trachea, yet that immune tolerance is compromised by the parasitic nematode Hp. Contact with either nematode species triggers epithelial reactive oxygen species (ROS) production in Ma. Only the entry of Bx, not Hp, infection, induces increased expression of antioxidative genes, through which the ROS levels are balanced in the trachea of beetles. Furthermore, we found that up‐regulation of antioxidative genes was induced by the interaction of Toll receptors. In contrast, beetles infected by Hp retain high levels of oxidative stress and melanization in trachea, and as a result, decrease Bx loading. This study highlights the role of Toll receptors in mediating the activation of antioxidative genes in immune tolerance to plant parasitic nematodes, and suggests the use of insect parasites as a biologic control.—Zhou, J., Zhao, L.‐L., Yu, H.‐Y., Wang, Y.‐H., Zhang, W., Hu, S.‐N., Zou, Z., Sun, J.‐H. Immune tolerance of vector beetle to its partner plant parasitic nematode modulated by its insect parasitic nematode. FASEB J. 32, 4862–4877 (2018). www.fasebj.org