Trichoderma harzianum induces resistance to root-knot nematodes by increasing secondary metabolite synthesis and defense-related enzyme activity in Solanum lycopersicum L

Abstract

Trichoderma spp. can improve plant defense against diverse plant pathogens, including fungi, bacteria, viruses, and nematodes. Nonetheless, the underlying mechanisms of Trichoderma-induced enhanced resistance, particularly against plant-parasitic root-knot nematodes (RKNs), remain poorly understood. Here, we show that T. harzianum (TH) could effectively suppress RKN (Meloidogyne incognita) infestation with an RKN reduction percentage of 61.88% in tomato plants (Solanum lycopersicum L.). While RKN infections increased the levels of reactive oxygen species (ROS; H2O2 and O2•‾) and lipid peroxidation in tomato roots, colonization with TH significantly reduced the levels of ROS, malondialdehyde, and electrolyte leakage, which was associated with increased accumulation of multiple secondary metabolites such as flavonoids, phenols, lignin, and cellulose on 75 days after inoculation with M. incognita. Consistent with the content of secondary metabolites, the activities of enzymes related to plant defense and the expression of associated genes (PAL, C4H, 4CL, CAD, LPO, CCOMT, Tpx1, and G6PDH) significantly increased in TH + RKN-inoculated roots compared with that in only RKN-treated roots. Moreover, TH inoculation prior to RKN infestation significantly increased the activity of pathogenesis-related (PR) proteins such as β-1,3-glucanase, chitinase, protease, and amylase by 86.31%, 36.25%, 39.78%, and 17.06%, respectively, compared with the RKN-infested roots. Furthermore, TH significantly stimulated the levels of salicylic acid and jasmonic acid. These results indicate a positive role of TH in inducing resistance against the RKNs by promoting secondary metabolism and the activity and transcripts of defense-related enzymes in tomato roots. Our study unveiled critical mechanisms of Trichoderma-induced improved resistance to RKNs, which can be useful for developing sustainable agricultural practices.