Trichoderma Counteracts the Challenge of Phytophthora nicotianae Infections on Tomato by Modulating Plant Defense Mechanisms and the Expression of Crinkler, Necrosis-Inducing Phytophthora Protein 1, and Cellulose-Binding Elicitor Lectin Pathogenic Effectors

Abstract

Decoding the mechanisms of plant defense against plant pathogens in a scenario where antagonistic activity and the plant growth-promoting effects of useful organisms intervene simultaneously is a new frontier of plant pathology. Here, we demonstrated that (i) two selected strains of <i>Trichoderma asperellum</i> and <i>Trichoderma atroviride</i> promoted tomato (<i>Solanum lycopersicum</i>) growth and reduced the severity of disease caused by the oomycete <i>Phytophthora nicotianae</i> and (ii) the genetic patterns of the components of the experimental model system tomato-<i>Trichoderma</i> spp.-<i>P. nicotianae</i> were differentially expressed. The beneficial effects in both the promotion of the growth of host plant and the biological control of the pathogen by two selected strains of different <i>Trichoderma</i> species were tested both <i>in planta</i> and <i>in vitro</i>. In both respects, <i>T. atroviride</i> demonstrated to be more effective than <i>T. asperellum</i>. Additionally, the simultaneous transcriptional reprogramming of several plant defense-related genes, pathogen effectors, and mycoparasitism-related genes in tomato, <i>P. nicotianae</i>, and <i>Trichoderma</i> spp., respectively, was evaluated during the three-component interaction. Results support the hypothesis that <i>Trichoderma</i> spp. elicit the expression of plant defense-related genes. As expected, a mycoparasitism-related gene was significantly up-regulated in <i>Trichoderma</i>-colonizing tomato plants infected by <i>P. nicotianae</i>. Finally, a marked up-regulation of the genes encoding two necrosis-inducing effectors was observed in <i>P. nicotianae</i> infecting tomato plants colonized by <i>Trichoderma</i>. In conclusion, this study is a contribution toward understanding the genetic pathways related with the ability of <i>Trichoderma</i> spp. to counteract the challenge of <i>P. nicotianae</i> infections on tomato. Additionally, the experiments revealed the beneficial effects in the tomato growth promotion of a new <i>T. atroviride</i> strain and its good antagonistic effectiveness in the biological control of root and crown rot incited by <i>P. nicotianae</i>, confirming that <i>Trichoderma</i> spp. can be a powerful tool in integrated pest management strategies of <i>Phytophthora</i> diseases of horticultural crops.