A soil fungus confers plant resistance against a phytophagous insect by disrupting the symbiotic role of its gut microbiota

Abstract

Plants generate energy flows through natural food webs, driven by competition for resources among organisms, which are part of a complex network of multitrophic interactions. Here, we demonstrate that the interaction between tomato plants and a phytophagous insect is driven by a hidden interplay between their respective microbiotas. Tomato plants colonized by the soil fungus Trichoderma afroharzianum , a beneficial microorganism widely used in agriculture as a biocontrol agent, negatively affects the development and survival of the lepidopteran pest Spodoptera littoralis by altering the larval gut microbiota and its nutritional support to the host. Indeed, experiments aimed to restore the functional microbial community in the gut allow a complete rescue. Our results shed light on a novel role played by a soil microorganism in the modulation of plant–insect interaction, setting the stage for a more comprehensive analysis of the impact that biocontrol agents may have on ecological sustainability of agricultural systems.

The sophisticated evolution of Trichoderma to control insect pests

“…The work described in Di Lelio et al. ( 5 ) reveals the intricate interkingdom relationships that can occur in natural and agricultural systems, and sheds light on a new aspect of the complex multitrophic interactions that will have a significant impact on the success of future biological control strategies.…”

“…Di Lelio et al. ( 5 ), in PNAS, describe how a multitrophic fungus–plant–animal–bacteria interaction ( Fig. 1 ) leads to a novel mechanism of Trichoderma -mediated insect pest biocontrol by modification of the bacterial microbiome in the phytophagous larvae feeding on leaves from a plant whose metabolome has been modified following Trichoderma colonization.…”

“…Di Lelio et al. ( 5 ) describe a trophic network-based crop protection mechanism underlying the insect biocontrol activity of Spodoptera littoralis moth larvae by a commercially recognized and registered biofungicide strain of Trichoderma afroharzianum , mediated by tomato-induced modifications of the insect’s gut microbiota. In brief, when tomato subapical leaves, from 4-wk-old plants emerging from seeds coated with T. afroharzianum spores, were ingested by S. littoralis larvae, there was a significantly negative impact observed on the survival, development, and longevity of the insect from the 4th larval (4th instar) to the pupation stage.…”

“…Thus, Di Lelio et al. ( 5 ) directed studies toward the influence of Trichoderma on the larval midgut and the colonizing microbiota. They further investigated in 4th instar larvae of S. littoralis : i) the transcriptional changes in midgut cells of larvae fed with leaves from plants inoculated and non-inoculated with T. afroharzianum , analyzing specifically the changes associated with digestive processes and membrane transporters involved in nutrient absorption, and ii) how Trichoderma could affect the plant metabolic processes that could modify the composition of the gut microbiome and its symbiotic contribution to larval nutrition.…”

“…Considering that the Trichoderma treatment caused strong perturbation of the transcriptional activity of microbiota associated with the biosynthesis of amino acids and the metabolism of sugars and ribonucleotides, Di Lelio et al. ( 5 ) suggested that the decline in the abundance of E. casseliflavus after the application of T. afroharzianum might lead to a reduced support of energy metabolism, largely dependent on amino acids and lipids. As a proof of concept, two rescue experiments were performed.…”