A novel plant "wire communication" process after infection by foliar necrotrophic pathogens: the first description of Trichoderma as an interplant communicator

For several decades, the question of how mycorrhizal fungi have the ability to colonize the roots of neighboring plants, connecting them through a fungal network, has been studied and demonstrated. This group of hyphae is used as a "wire communication" between plants that allows the transmission of signals between plants regarding biotic (pathogens and pests) and even abiotic (fire) stresses, widely known as "the internet of forests". Although this mechanism is widely known in mycorrhizal fungi, it has not been described in other groups of fungi, such as endophytic fungi. Within this group, Trichoderma is a genus of filamentous fungi widely studied and used as a biological control agent in agriculture, with no capacity described so far as an inter-plant communicator. To study this possibly biological phenomenon, we used the model plant Arabidopsis thaliana, the species Trichoderma hamatum, isolated from kale roots (Brassica oleracea var. acephala), and the pathogens Sclerotinia sclerotiorum and Xanthomnas campestris (necrotrophic fungus and hemibiotrophic bacterium, respectively). Through the analysis of foliar infection by pathogens, root colonization by Trichoderma and systemic plant defense responses, we have been able to identify for the first time the ability of Trichoderma to act as an inter-plant communicator. This is due to a systemic foliar increase of jasmonic acid-mediated defenses, which cause an antagonistic increase in salicylic-acid-mediated defenses in roots. In turn, root defenses control and respond to Trichoderma colonization levels, a mechanism used by the fungus to signal between neighboring plants. However, it is important to note that this mechanism only works with necrotrophic pathogens, without developing in response to the hemibiotrophic pathogen.