The Dark Side of Antioxidants: When Scavenging ROS Undermines Plant Stress Acclimation

Reactive oxygen species (ROS) exert dual biological functions in plants. Though they form toxic byproducts of aerobic metabolism, ROS also serve as indispensable secondary messengers that orchestrate stress acclimation programs. For decades, plant physiologists operated under a pervasive assumption that constitutive and non-compartmentalized upregulation of antioxidant capacity would universally enhance abiotic stress tolerance. This long-standing dogma has now been thoroughly overturned. A growing body of evidence shows that sustained, global high antioxidant activity often impairs adaptation rather than helping it. In this review, we replace the simplistic “more antioxidants equal better tolerance” framework with a dynamic model of cellular redox homeostasis. We dissect three interconnected mechanisms though which unrestrained ROS scavenging generates deleterious phenotypic outcomes. First, indiscriminate clearance blunts transient ROS pulses and propagating ROS waves, the core signaling events acquired to trigger systemic acquired acclimation (SAA). Second, continuous antioxidant biosynthesis drains finite carbon skeletons, NADPH, and ATP pools, exacerbating evolutionary growth-defense resource trade-offs. Third, non-specific bulk ROS scavenging erases compartment-specific organellar retrograde signals, which rely on tightly controlled spatial and temporal ROS fluctuations. We concurrently define physiological boundary conditions where robust antioxidant activity remains vital for plant survival under extreme stress. Rather than advocating for the complete suppression of ROS detoxification, our analysis advocates context-dependent fine-tuning of redox signaling networks. We also summarize emerging precision redox monitoring and genetic engineering tools, and outline translational breeding pipelines to develop climate-resilient crops that balance stress survival and yield stability. This work delivers novel conceptual perspectives to advance fundamental plant redox biology.