The secret life of insect-associated microbes and how they shape insect-plant interactions

Abstract

Insects are associated with a plethora of different microbes of which we are only starting to understand their role in shaping insect-plant interactions. Besides directly benefitting from symbiotic microbial metabolism, insects obtain and transmit microbes within their environment, making them ideal vectors and potential beneficiaries of plant diseases and microbes that alter plant defenses. To prevent damage, plants elicit stress-specific defenses to ward off insects and their microbiota. However, both insects and microbes harbor a wealth of adaptations that allow them to circumvent effective plant defense activation. In the past decades, it has become apparent that the enormous diversity and metabolic potential of insect-associated microbes may play a far more important role in shaping insect-plant interactions than previously anticipated. The latter may have implications for the development of sustainable pest control strategies. Therefore, this review sheds light on the current knowledge on multitrophic insect-microbe-plant interactions in a rapidly expanding field of research.

Keywords: insects; insect–microbe–plant interactions; microbiota; pathogens; plant defenses; symbionts.

Figure 1.

Overview of insect-associated microbe interference with plant defense signaling. Plant stress perception leads to the activation of receptor-like cytoplasmic kinases (RLCKs), mitogen activated kinases (MAPKs), and Ca²⁺ influx, which in turn results in the activation of calcium-dependent protein kinases (CPKs). Ca²⁺, RLCKs, and CPKs are involved in the activation of RbohD, which produces extracellular reactive oxygen species (ROS) that together with Ca²⁺ acts as second messenger in systemic signaling throughout the plant. Activation of CPKs, RLCKs, and MAPKs leads to downstream stress signaling, involving the activation of transcription factors that regulate the production of phytohormones and secondary metabolites. Crosstalk between (phytohormonal) signaling pathways is further explained in the main text. ABA, abscisic acid; AUX, auxin; BR, brassinosteroids; CK, cytokinins; ET, ethylene; GA, gibberellin; JA, jasmonic acid; LPS, lipopolysaccharides; PG, peptidoglycan; SA, salicylic acid; and SL, strigolactones.

Figure 2.

Schematic overview of major induced systemic plant defense pathways. Herbivorous insects induce damage or herbivore (DAMP/HAMP)-induced resistance (in yellow) in plants that gives rises to defense priming for jasmonic acid (JA), abscisic acid (ABA), and ethylene (ET). Herbivore-triggered resistance also involves the production of herbivore-induced plant volatile emission that attracts insect parasitoids that parasitize insects. Pathogenic microbes, that are often transmitted by insects, can trigger plant PAMP-induced systemic acquired resistance (SAR, in red) that primes plant defenses for salicylic acid (SA). Plant beneficial soil-microbes, potentially transmitted by insects, can give rise to induced systemic resistance (ISR) that primes plants for JA and ethylene defenses and subsequent release of volatiles. Infected or infested plants also recruit beneficial microbes that protect next generations of plants against infestation via a microbial soil legacy through plant–soil feedback.