Enrique Monte

PNAS March 13, 2023; 120 (12) e2301971120

https://doi.org/10.1073/pnas.2301971120

Figure: Larva of S. littoralis on Solanum lycopersicum. Gut dysbiosis in insect larvae feeding on leaves from plants treated with Trichoderma.

Trichoderma (Ascomycota, teleomorph: Hypocrea) is comprised of species that are multipurpose, plant-beneficial fungi with importance in agriculture as a direct biological control agent (BCA). However, due to its interaction with plants, it has become recognized also as an indirect BCA and a biostimulant, permitting reduced applications of agrochemicals, thus promoting an ecosustainable agriculture (1). Phylogenomic analysis has shown that the genus shared a last common ancestor with entomoparasitic hypocrealean fungi (e.g., Cordyceps, Beauveria) and evolved from a predecessor with limited cellulolytic capability that fed on either fungi or arthropods (2). Trichoderma evolution was subsequently directed toward successive host shifts combining mycotrophy and phytophagy (3), and it is widely accepted that mycoparasitism is the ancestral lifestyle of the genus (4). However, direct activity against insects, together with indirect biocontrol via activation of plant defenses or attraction of insect pest enemies, either by Trichoderma-produced metabolites or induced phytocompound release from the plant by this fungus, are traits that the species of Trichoderma have retained and acquired during its evolutionary leaps (1). 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.

Results indicated that plants treated with Trichoderma had a lower abundance of fatty acids and amino acid content, increased accumulation of glycogen, and activated oxidative processes and antibacterial immune genes, findings that suggest the existence of an imbalance (dysbiosis) in the functional composition and metabolic activities of the gut microbiota following the ingestion of leaves from the Trichoderma treatment. 

Trichoderma has evolved to mediate gut dysbiosis in insect larvae feeding on leaves from plants treated with the BCA itself. 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.

See https://www.pnas.org/doi/10.1073/pnas.2301971120