Reactive oxygen species and secondary metabolite nexus in plant-microbe dialogues

Plants interact continuously with diverse microbial communities ranging from mutualists to pathogens. Reactive oxygen species (ROS) and secondary metabolites (SMs) are central regulators of these interactions, functioning as interconnected signaling and defense components. ROS coordinate pattern-triggered immunity (PTI), effector-triggered immunity (ETI), systemic signaling, and cellular reprogramming, whereas SMs such as phenolics, terpenoids, and alkaloids contribute to antimicrobial defense, signaling, and plant–microbe specificity. In this tightly interconnected nexus, ROS regulate SM biosynthetic pathways, while SMs modulate ROS homeostasis through antioxidant and signaling functions. This bidirectional crosstalk therefore helps determine interaction outcomes by balancing defense activation, metabolic cost, and symbiotic compatibility. Furthermore, microbial modulation of ROS–SM networks is highly context-dependent. Pathogens may suppress or detoxify early immune-associated ROS to facilitate colonization, whereas some later exploit ROS accumulation and host cell death depending on trophic lifestyle and infection stage. Beneficial microbes can likewise induce, attenuate, or spatially regulate ROS and SM responses during colonization, accommodation, and immune priming. Thus, the outcome of plant–microbe interactions depends on microbial identity and lifestyle together with the magnitude, duration, and localization of host redox responses. This review synthesizes current knowledge of ROS–SM crosstalk in plant–microbe interactions, emphasizing biochemical sources, regulatory networks, microbial manipulation, and systemic functions. We also highlight emerging insights from multi-omics, spatial biology, and systems modeling, and discuss opportunities to harness ROS–SM networks for sustainable crop protection, microbiome engineering, and climate-resilient agriculture.