Thermal energy dissipation in reaction centres and in the antenna of photosystem II protects desiccated poikilohydric mosses against photo-oxidation

Abstract

Seasonal differences have been observed in the ability of desiccated mosses to dissipate absorbed light energy harmlessly into heat. During the dry summer season desiccation-tolerant mosses were more protected against photo-oxidative damage in the dry state than during the more humid winter season. Investigation of the differences revealed that phototolerance could be acquired or lost even under laboratory conditions. When a desiccated poikilohydric moss such as Rhytidiadelphus squarrosus is in the photosensitive state, the primary quinone, Q(A), in the reaction centre of photosystem II is readily reduced even by low intensity illumination as indicated by reversibly increased chlorophyll fluorescence. No such reduction is observed even under strong illumination in desiccated mosses after phototolerance has been acquired. In this state, reductive charge stabilization is replaced by energy dissipation. As a consequence, chlorophyll fluorescence is quenched. Different mechanisms are responsible for quenching. One is based on the presence of zeaxanthin provided drying occurs in the light. This mechanism is known to be controlled by a protonation reaction which is based on proton-coupled electron transport while the moss is still hydrated. Another mechanism which also requires light for activation, but no protonation, is activated during desiccation. While water is slowly lost, fluorescence is quenched. In this situation, an absorption band formed at 800 nm in the light is stabilized. It loses reversibility on darkening. Comparable kinetics of fluorescence quenching and 800 nm signals as well as the linear relationship between non-photochemical fluorescence quenching (NPQ) and loss of stable charge separation in photosystem II reaction centres suggested that desiccation-induced quenching is a property of photosystem II reaction centres. During desiccation, quenchers accumulate which are stable in the absence of water but revert to non-quenching molecular species on hydration. Together with zeaxanthin-dependent energy dissipation, desiccation-induced thermal energy dissipation protects desiccated poikilohydric mosses against photo-oxidation, ensuring survival during drought periods.