Rewiring the proteome of the Euscelidius variegatus holobiont in response to Flavescence dorée phytoplasma

The leafhopper Euscelidius variegatus is a laboratory vector of the phytoplasma associated to Flavescence dorée, a severe grapevine disease that threatens viticulture in Europe. Transcriptomic studies have already provided valuable insights into the mechanisms of insect-phytoplasma interactions, but proteomics can offer immediate insights into the cellular functions and metabolic adaptations of the insect and its microbiome to the presence of this plant bacterium. Here, the generation of new genomic data of the E. variegatus holobiont was instrumental in elaborating the first comprehensive proteomic profile of its response to Flavescence dorée phytoplasma (FDp). Both data-dependent acquisition and data-independent acquisition mass spectrometry were used to explore the complex molecular interactions between the insect host, its microbial community, and the phytoplasma. Results indicated a critical role of the insect mitochondria as a shared interface exploited by phytoplasmas for survival and propagation. Additionally, it appeared that the presence of FDp had a detrimental impact on the reciprocal metabolic support between the insect host and its two primary endosymbionts, predominantly resulting in a perturbation in amino acid synthesis and exchange. Proteins upregulated in response to FDp may represent promising targets for disrupting phytoplasma acquisition and transmission, either through rationally designed agrochemicals or gene silencing approaches.