<i>Trichoderma harzianum</i> Improves Defense Against <i>Fusarium oxysporum</i> by Regulating ROS and RNS Metabolism, Redox Balance, and Energy Flow in Cucumber Roots

Abstract

Plant survival in the terrestrial ecosystem is influenced by both beneficial and harmful microbes. <i>Trichoderma</i> spp. are a group of filamentous fungi that promote plant growth and resistance to harmful microbes. Previously, we showed that the genus <i>Trichoderma</i> could effectively suppress Fusarium wilt in cucumber. However, the mechanisms that underlie the effects of the genus <i>Trichoderma</i> on plant defense have not been fully substantiated. Two essential metabolic pathways, such as the ascorbate (AsA)-glutathione (GSH) cycle and the oxidative pentose phosphate pathway (OPPP), have been shown to participate in plant tolerance to biotic stressors; nevertheless, the involvement of these pathways in <i>Trichoderma</i>-induced enhanced defense remains elusive. Here, we show that <i>Trichoderma harzianum</i> could alleviate oxidative and nitrostative stress by minimizing reactive oxygen species (ROS; hydrogen peroxide and superoxide) and reactive nitrogen species (nitric oxide [NO]) accumulation, respectively, under <i>Fusarium oxysporum</i> infection in cucumber roots. The genus <i>Trichoderma</i> enhanced antioxidant potential to counterbalance the overproduced ROS and attenuated the transcript and activity of NO synthase and nitrate reductase. The genus <i>Trichoderma</i> also stimulated <i>S</i>-nitrosylated glutathione reductase activity and reduced <i>S</i>-nitrosothiol and <i>S</i>-nitrosylated glutathione content. Furthermore, the genus <i>Trichoderma</i> enhanced AsA and GSH concentrations and activated their biosynthetic enzymes, γ-GCS and l-galactono-1,4-lactone dehydrogenase. Interestingly, the genus <i>Trichoderma</i> alleviated <i>Fusarium</i>-inhibited activity of glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase, enzymes involved in the OPPP. Such positive regulation of the key enzymes indicates the adequate maintenance of the AsA-GSH pathway and the OPPP, which potentially contributed to improve redox balance, energy flow, and defense response. Our study advances the current knowledge of <i>Trichoderma</i>-induced enhanced defense against <i>F. oxysporum</i> in cucumber.