Energy Dissipation and Photoinhibition: A Continuum of Photoprotection

Abstract

Summary The photosynthetic apparatus is exquisitely adapted to capture light energy and convert it into reduced carbon compounds while also protecting against the potential deleterious effects of excessive excitation energy. The latter is achieved through fine regulation of thermal energy dissipation over multiple time scales and in response to many different environmental stresses. Over short time scales in the absence of additional stress, control is exerted through pH regulation of the enzymatic conversion of violaxanthin to zeaxanthin (and its return to violaxanthin) and engagement of zeaxanthin in thermal energy dissipation. Under more extreme exposure to excess light (transfer of shade leaves to high light or the imposition of additional stresses in the presence of high light), greater levels of zeaxanthin are retained and may also be maintained in a dissipative configuration even in darkness. Engagement of zeaxanthin in thermal energy dissipation lowers the maximal efficiency of photosystem II (PS II) as the excess excitation energy is diverted away from the reaction centers and harmlessly released as heat. Thus, maximal PS II efficiency exhibits decreases and increases with varying degrees of light absorption. Under prolonged and/or pronounced exposure to excess light, maximal PS II efficiency can furthermore exhibit nocturnally sustained decreases as the potential for photoprotective zeaxanthin-dependent energy dissipation is maintained. Zeaxanthin-dependent energy dissipation that is sustained at moderate temperatures is also typically accompanied by downregulation of photosynthesis, including photosynthetic electron transport. Decreases in photosynthetic electron transport presumably lower the likelihood of electrons reducing molecular oxygen to superoxide, and sustained zeaxanthin-dependent energy dissipation mitigates the formation of singlet excited oxygen. Thus, while sustained decreases in maximal PS II efficiency and photosynthetic capacity are key characteristics of photoinhibition, they are also the features that provide powerful photoprotection against the formation of toxic reactive oxygen species.