Trichoderma harzianum improves defense against Fusarium oxysporum by regulating ROS and RNS metabolism, redox balance and energy flow in cucumber roots.

Plant survival in the terrestrial ecosystem is influenced by both beneficial and harmful microbes. Trichoderma spp. are a group of filamentous fungi that promote plant growth and resistance to harmful microbes. Previously, we showed that Trichoderma could effectively suppress Fusarium wilt in cucumber. However, the mechanisms that underlie the effects of Trichoderma on plant defense have not been fully substantiated. Recently, two essential metabolic pathways such as ascorbate (AsA)-glutathione (GSH) cycle and oxidative pentose phosphate pathway (OPPP) have been shown to participate in plant tolerance to biotic stressors, nevertheless, the involvement of these pathways in Trichoderma-induced enhanced defense remains elusive. Here, we show that Trichoderma harzianum could alleviate oxidative and nitrostative stress by minimizing reactive oxygen species (ROS, H2O2 and O2●-) and reactive nitrogen species (RNS, NO) accumulation, respectively under Fusarium oxysporum infection in cucumber roots. Trichoderma enhanced antioxidant potential to counterbalance the overproduced ROS and attenuated the transcript and activity of NO synthase (NOS) and nitrate reductase (NR). Trichoderma also stimulated S-nitrosylated glutathione reductase (GSNOR) activity and reduced S-nitrosothiol (SNO) and S-nitrosylated glutathione (GSNO) content. Furthermore, Trichoderma enhanced AsA and GSH concentrations, and activated their biosynthetic enzymes, γ-GCS and GaILDH. Interestingly, Trichoderma alleviated Fusarium-inhibited activity of G6PDH and 6PGDH, enzymes involved in OPPP. Such positive regulation of the key enzymes indicates the adequate maintenance of AsA-GSH and OPP pathways, which potentially contributed to improve redox balance, energy flow and defense response. Our study advances the current knowledge of Trichoderma-induced enhanced defense against F. oxysporum in cucumber.