Unlocking agro-ecosystem sustainability: exploring the bottom-up effects of microbes, plants, and insect herbivores

Agricultural ecosystem formation and evolution depend on interactions and communication between multiple organisms. Within this context, communication occurs between microbes, plants, and insects, often involving the release and perception of a wide range of chemical cues. Unraveling how this information is coded and interpreted is critical to expanding our understanding of how agricultural ecosystems function in terms of competition and cooperation. Investigations examining dual interactions (e.g. plant-microbe, insect-microbe, and insect-plant) have resolved some basic components of this communication. However, there is a need for systematically examining multitrophic interactions that occur simultaneously between microorganisms, insects, and plants. A more thorough understanding of these multitrophic interactions has been made possible by recent advancements in the study of such ecological interactions, which are based on a variety of contemporary technologies such as artificial intelligence sensors, multi-omics, metabarcoding, and others. Frequently, these developments have led to the discovery of startling examples of each member manipulating the other. Here, we review recent advances in the understanding of bottom-up chemical communication between microorganisms, plants, and insects, and their consequences. We discuss the components of these "chemo-languages" and how they modify outcomes of multi-species interactions across trophic levels. Further, we suggest prospects for translating the current basic understanding of multitrophic interactions into strategies that could be applied in agricultural ecosystems to increase food safety and security.