Trichoderma hamatum can act as an inter-plant communicator of foliar pathogen infections by colonizing the roots of nearby plants: A new inter-plant “wired communication”

Abstract

Trichoderma is a genus of filamentous fungi widely studied and used as a biological control agent in agriculture. However, its ability to form fungal networks for inter-plant communication by means of the so-called inter-plant "wired communication" has not yet been addressed. In our study we used the model plant Arabidopsis thaliana, the fungus Trichoderma hamatum (isolated from Brassicaceae plants) and the pathogens Sclerotinia sclerotiorum and Xanthomonas campestris (necrotrophic fungus and hemibiotrophic bacteria, respectively). We performed different combinations of isolated/neighboring plants and root colonization/non-colonization by T. hamatum, as well as foliar infections with the pathogens. In this way, we were able to determine how, in the absence of T. hamatum, there is an inter-plant communication that induces systemic resistance in neighboring plants of plants infected by the pathogens. On the other hand, the plants colonized by T. hamatum roots show a greater systemic resistance against the pathogens. Regarding the role of T. hamatum as an inter-plant communicator, it is the result of an increase in foliar signaling by jasmonic acid (increased expression of LOX1 and VSP2 genes and decreased expression of ICS1 and PR-1 genes), antagonistically increasing root signaling by salicylic acid (increased expression of ICS1 and PR-1 genes and decreased expression of LOX1 and VSP2). This situation prevents root colonization by T. hamatum of the foliarly infected plant and leads to massive colonization of the neighboring plant, where jasmonic acid-mediated systemic defenses are induced.