Non-photochemical energy dissipation in dynamic natural environments

Sunlight harnessed by photosynthesis is the ultimate energy source for virtually all life on earth as well as a source of essential information for the plant through signaling based on reactive oxygen species (ROS). Photosynthesis thus requires protection against excess excitation without interference with vital ROS-based messages. This review focuses on the ubiquitous, highly malleable mechanism for modulating excitation level via non-photochemical energy dissipation assessed from non-photochemical quenching (NPQ) of chlorophyll fluorescence. We evaluate energy dissipation across a wide range of ecosystems to assess how timing and severity of environmental stress as well as plant lifeform determine energy-dissipation type employed; pH-dependent dissipation is associated with continued growth under mild to moderate stress, whereas pH-independent dissipation supports survival under severe stress to enable growth resumption post-stress. We also give attention to links between energy dissipation and biotic stress defenses as well as regulation of lifecycle progression. We highlight that excess excitation and energy dissipation are part of the daily routine wherever plants grow naturally and that experimental plants grown under low light (i.e., without acclimation to excess light) do not disclose their full photoprotective capability as relevant to natural settings including agriculture. We summarize what standard NPQ measurements can and cannot reveal. Overall, the findings presented illustrate that what makes a "better" plant in some natural settings might be a liability in other settings and that outcomes of efforts to engineer NPQ will be highly dependent on environmental context.