Antioxidant systems modulate oxidant-based signaling networks and excessive removal of oxidants can prevent beneficial acclimation responses. Evidence from mutant, transgenic, and locally adapted natural plant systems is used to interpret differences in the capacity for antioxidation and formulate hypotheses for future inquiry. We focus on the first line of chloroplast antioxidant defense, pre-emptive thermal dissipation of excess absorbed light (monitored as nonphotochemical fluorescence quenching, NPQ) as well as on tocopherol-based antioxidation. Findings from NPQ-deficient and tocopherol-deficient mutants that exhibited enhanced biomass production and/or enhanced foliar water-transport capacity are reviewed and discussed in the context of the impact of lower levels of antioxidation on plant performance in hot/dry conditions, under cool temperature, and in the presence of biotic stress. The complexity of cellular redox-signaling networks is related to the complexity of environmental and endogenous inputs as well as to the need for intensified training and collaboration in the study of plant–environment interactions across biological sub-disciplines.