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 vector beetle 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.

Mitogenome Analysis of Four Lamiinae Species (Coleoptera: Cerambycidae) and Gene Expression Responses by Monochamus alternatus When Infected with the Parasitic Nematode, Bursaphelenchus mucronatus

“…Some previous studies have already shown that the expression of several genes in M. alternatus was altered when infected by B. xylophilus . For example, Zhou et al [ 31 ] showed that in order to obtain immune tolerance, M. alternatus infected with B. xylophilus would induce an increase in the expression of antioxidant genes. Through the increased expression of these antioxidant genes, the level of ROS in the trachea of longicorn beetles increases and reaches a state of equilibrium [ 31 ].…”

“…For example, Zhou et al [ 31 ] showed that in order to obtain immune tolerance, M. alternatus infected with B. xylophilus would induce an increase in the expression of antioxidant genes. Through the increased expression of these antioxidant genes, the level of ROS in the trachea of longicorn beetles increases and reaches a state of equilibrium [ 31 ]. Coincidentally, as one of the main sources of ROS, the genes ND4 and ND5 , which code for two subunits of Complex I, were found to be significantly up-regulated in this study.…”

“…There have already been several studies related to mitochondrial gene expression [ 27 , 28 , 29 , 30 ]. Previous studies have already demonstrated that gene expression in M. alternatus was different when infected with B. xylophilus [ 31 , 32 ]. Zhou et al [ 31 ] proved that M. alternatus infected with B. xylophilus showed an increase in the expression of antioxidant genes in order to obtain immune tolerance.…”

“…Previous studies have already demonstrated that gene expression in M. alternatus was different when infected with B. xylophilus [ 31 , 32 ]. Zhou et al [ 31 ] proved that M. alternatus infected with B. xylophilus showed an increase in the expression of antioxidant genes in order to obtain immune tolerance. In addition, Ning et al [ 32 ] found that there were many differentially expressed microRNAs (miRNAs) in M. alternatus with nematode infections and the expression of neuron-related miRNAs increased significantly.…”

Gene family expansion of pinewood nematode to detoxify its host defence chemicals

“…Nematodes inhabit a diversity of habitats and can be free‐living ( Caenorhabditis elegans and C. briggsae ), animal‐parasitic ( Strongyloides stercoralis in mammals, Brugia malayi and Enterobius vermicularis in humans) and plant‐parasitic ( Meloidogyne incognita and M. hapla in many crops and Globodera pallida in potatoes among others) (Coghlan, ). Consequently, nematodes experience a much greater array of deleterious xenobiotic exposure in soils (Lindblom & Dodd, ) and insect haemolymph (Zhou et al, ) and to plant defence chemicals (Niu, Zhao, Lu, Zhang, & Sun, ). Thus, xenobiotic detoxification is necessary for survival.…”