The role of GPCRs in metabolism and physiology of the pea aphid, Acyrthosiphon pisum.

Insects comprise 80% of the world’s animal species representing the largest and most diverse life form on the planet. Over evolutionary time, insects occupied and adapted to widely divergent habitats, resulting in a rich variation of body plans with different shapes, sizes, and specialized feeding mechanisms. They thus represent a unique opportunity to gain insight in the mechanisms that control feeding and metabolism and how they change during evolution. In addition, understanding the regulation of feeding provides an opportunity to identify novel approaches that can be used for targeted control of insects, our main competitors for food. The order of Hemiptera, also known as the true bugs, is ranked in the top three of important pest insects. Hemiptera feed on fluids for which they use modified mouthparts, including a stylet. A well-known group of Hemiptera are the aphids. Plant phloem sap, the exclusive food source for aphids, contains a high concentration of carbohydrates, but it lacks or is low in several essential amino acids and vitamins. The nutritional requirements needed for aphid development and reproduction are met thanks to the evolutionary ancient relationship with the endosymbiotic bacterium, Buchnera aphidicola. These bacteria are located in large specialized cells within the aphid, known as bacteriocytes. Initially, it was thought that the sole function of the bacteriocytes was to house the bacteria, but recent work demonstrated remarkable dynamics and plasticity of bacteriocytes. This raises the question of how bacteriocytes are integrated in and regulated by host physiology and metabolism. GPCRs are the largest group of transmembrane proteins and mediate many important physiological and behavioral processes. To date, many insect neuropeptides and GPCRs are known to regulate feeding behavior and gut motility. However, little to nothing is known about the role of GPCRs in regulating feeding and metabolism in aphids.

In this study, we will use the pea aphid, Acyrthosiphon pisum, as a model insect to identify and characterize GPCRs with roles in feeding and metabolic homeostasis. We will focus on key tissues in aphid feeding and nutrition-related metabolism, the gut and bacteriocytes.

The project consists of two main parts, the analysis of peptide ligand specificity and characterization of the role of GPCRs in nutrient-dependent metabolism and physiology. Relevant GPCRs have been selected based on their expression within the tissues of interest, gut and bacteriocytes. First, the ligand specificity will be determined in heterologous cell lines. Subsequently, the physiological response of gut and bacteriocytes to ligand binding will be determined in in vitro systems. Second, all GPCRs and their ligands will systematically be targeted with RNAi and peptidomimetics through feeding to identify antifeedant activity and determine their role in aphid physiology and metabolism.

This research will give us more insight in the role of GPCRs in regulating feeding and metabolism in aphids and in how the bacteriocytes are integrated in the pea aphid interorgan communication network that regulates metabolic homeostasis. This work may also lead to the identification of new targets for pest insect control.