The interactions of Trichoderma at multiple trophic levels: inter-kingdom communication

Trichoderma spp. are universal saprotrophic fungi in terrestrial ecosystems, and as rhizosphere inhabitants, they mediate interactions with other soil microorganisms, plants, and arthropods at multiple trophic levels. In the rhizosphere, Trichoderma can reduce the abundance of phytopathogenic microorganisms, which involves the action of potent inhibitory molecules, such as gliovirin and siderophores, whereas endophytic associations between Trichoderma and the seeds and roots of host plants can result in enhanced plant growth and crop productivity, as well as the alleviation of abiotic stress. Such beneficial effects are mediated via the activation of endogenous mechanisms controlled by phytohormones such as auxins and abscisic acid, as well as by alterations in host plant metabolism. During either root colonization or in the absence of physical contact, Trichoderma can trigger early defense responses mediated by Ca2+ and reactive oxygen species, and subsequently stimulate plant immunity by enhancing resistance mechanisms regulated by the phytohormones salicylic acid, jasmonic acid, and ethylene. In addition, Trichoderma release volatile organic compounds and nitrogen or oxygen heterocyclic compounds that serve as signaling molecules, which have effects on plant growth, phytopathogen levels, herbivorous insects, and at the third trophic level, play roles in attracting the natural enemies (predators and parasitoids) of herbivores. In this paper, we review some of the most recent advances in our understanding of the environmental influences of Trichoderma spp., with particular emphasis on their multiple interactions at different trophic levels.