Unraveling the link between epigenetics and insect symbiosis – Unleash

Weevils are common crop pests that thrive on nutritionally poor diets, and rely on intracellular symbiotic bacteria (endosymbionts) that supply them with nutrients lacking in their habitats. While many studies have focused on the impact of symbiosis on the endosymbiont genome, as for instance the drastically reduced genome size of the endosymbiont compared to free-living bacteria, very little is known on the host point of view. The main goal of this proposal is to understand the impact of symbiosis on the host genome, and most precisely on the host epigenetic mechanisms. There are three main epigenetic mechanisms: DNA methylation, chromatin remodeling factors as histone post-translational modifications and small RNAs. Despite being thoroughly studied in many model systems, the role of epigenetic pathways in the host-symbiont dialogue remains elusive. Because epigenetic is labile to environment changes, we hypothesize that a biotic stress, illustrated by the endosymbiont-host relationship, may modulate host epigenetic mechanisms and in consequence, host gene expression. In order to illustrate such biotic stress, we will study the mutualistic associatin between the cereal weevil, Sitophilus oryzae and its recently established endosymbiont Sodalis pierantonius. Firstly, tissue specific epigenetic knock down mutants illustrating both DNA methylation and small RNA epigenetic pathways will be generated. Then, differences in endosymbiont dynamics will be assayed and compared between mutants and wild type. If any epigenetic factor studied is crucial in the host-endosymbiont dialogue, it will be exposed in this first step. In addition, it will allow us to determine if symbiotic evolutionary constraints have global impact on host epigenetic mechanisms or if only a handful of host candidate genes are modulated through such mechanisms in response to symbiosis. Either case scenario will yield host candidate genes and small RNAs that might be responsible for the molecular dialogue between host and endosymbiont. The role of such candidates in symbiont dynamics will be tested by disrupting their expression using once again knock down mutants. Hence, we will be able to pinpoint key genes that are modulated through epigenetic regulation during symbiosis establishment. Finally, we will test the specificity of the epigenetic pathways uncovered regarding the endosymbiont, by analyzing weevils infected with different bacteria. This ambitious proposal aims at developing a new field of research, Epigenetics of Endosymbiosis and will benefit a large field of research encompassing insect biology, ecology and evolution. Finally, this proposal will shed light into key players in S. oryzae obligatory endosymbiont tolerance and maintenance and hence might be of interest to contain crop infections and decrease weevil’s economic burden.