Members of the fungal genus Trichoderma (Ascomycota, Hypocreales, Hypocreaceae) are ubiquitous and commonly encountered as soil inhabitants, plant symbionts, saprotrophs, and mycoparasites. Certain species have been used to control diverse plant diseases and mitigate negative growth conditions. The versatility of Trichoderma’s interactions mainly relies on their ability to engage in inter- and cross-kingdom interactions. Although Trichoderma is by far the most extensively studied fungal biocontrol agent (BCA), with a few species already having been commercialized as bio-pesticides or bio-fertilizers, their wide application has been hampered by an unpredictable efficacy under field conditions. Deciphering the dialogues within and across Trichoderma ecological interactions by identification of involved effectors and their underlying effect is of great value in order to be able to eventually harness Trichoderma’s full potential for plant growth promotion and protection. In this review, we focus on the nature of Trichoderma interactions with plants and pathogens. Better understanding how Trichoderma interacts with plants, other microorganisms, and the environment is essential for developing and deploying Trichoderma-based strategies that increase crop production and protection.

Certain Trichoderma strains protect plants from diverse pathogens using multiple mechanisms. We report a novel mechanism that may potentially play an important role in Trichoderma-based biocontrol. Trichoderma virens and T. viride significantly increased the amount/activity of secreted antifungal metabolites in response to volatile compounds (VCs) produced by 13 strains of Fusarium oxysporum, a soilborne fungus that infects diverse plants. This response suggests that both Trichoderma spp. recognize the presence of F. oxysporum by sensing pathogen VCs and prepare for attacking pathogens. However, T. asperellum did not respond to any, while T. harzianum responded to VCs from only a few strains. Gene expression analysis via qPCR showed up-regulation of several biocontrol-associated genes in T. virens in response to F. oxysporum VCs. Analysis of VCs from seven F. oxysporum strains tentatively identified a total of 28 compounds, including six that were produced by all of them. All four Trichoderma species produced VCs that inhibited F. oxysporum growth. Analysis of VCs produced by T. virens and T. harzianum revealed the production of compounds that had been reported to display antifungal activity. F. oxysporum also recognizes Trichoderma spp. by sensing their VCs and releases VCs that inhibit Trichoderma, suggesting that both types of VC-mediated interaction are common among fungi.

Diverse fungi are intimately associated with plants, and molecules secreted from both the plant and fungal sides play critical roles in the establishment of their associations and affect plant growth and health. Through evolutionary arms races or strategic alliances with plants, fungi and other microbes have invented a bewildering array of secreted molecules to parasitize or communicate with plants. Research empowered by omics data and tools has greatly advanced understanding of the nature, role and mechanism of action of many secreted fungal proteins that affect plants directly or indirectly. However, available information about fungal volatile metabolites with similar functions is quite limited. Through this review, we aim to stimulate expeditions to this vastly under-explored frontier of fungal chemical ecology.