Conservation and dissipation of light energy in desiccation-tolerant photoautotrophs, two sides of the same coin

Abstract

Conservation of light energy in photosynthesis is possible only in hydrated photoautotrophs. It requires complex biochemistry and is limited in capacity. Charge separation in reaction centres of photosystem II initiates energy conservation but opens also the path to photooxidative damage. A main mechanism of photoprotection active in hydrated photoautotrophs is controlled by light. This is achieved by coupling light flux to the protonation of a special thylakoid protein which activates thermal energy dissipation. This mechanism facilitates the simultaneous occurrence of energy conservation and energy dissipation but cannot completely prevent damage by light. Continuous metabolic repair is required to compensate damage. More efficient photoprotection is needed by desiccation-tolerant photoautotrophs. Loss of water during desiccation activates ultra-fast energy dissipation in mosses and lichens. Desiccation-induced energy dissipation neither requires a protonation reaction nor light but photoprotection often increases when light is present during desiccation. Two different mechanisms contribute to photoprotection of desiccated photoautotrophs. One facilitates energy dissipation in the antenna of photosystem II which is faster than energy capture by functional reaction centres. When this is insufficient for full photoprotection, the other one permits energy dissipation in the reaction centres themselves.

Chloroplast Genome Analysis of Resurrection Tertiary Relict Haberlea rhodopensis Highlights Genes Important for Desiccation Stress Response

“…In addition to its homoiochlorophyllous nature, H. rhodopensis has the capability of resurrection (survival of extreme vegetative dehydration), a trait that is of significant importance in global climate change. Desiccation tolerance is one of the most widely described traits studied in this paleoendemic species, and previous studies have shown that light absorption and oxygen intake evolution play a key role in the adaptation of this species to desiccation stress ( Heber et al, 2007 ; Heber, 2012 ). Drought resistance and rapid recovery of H. rhodopensis after rehydration were attributed to specific characteristics of the chloroplast of this species, including unchanged chlorophyll content, maintenance of chlorophyll–protein complexes, reversible modifications in PSII electron transport, and enhanced dissipation of non-radiative energy ( Georgieva et al, 2007 ; Mihailova et al, 2011 ).…”

An easily reversible structural change underlies mechanisms enabling desert crust cyanobacteria to survive desiccation

“…[1][2][3][4]). During the process of desiccation, continued photosynthetic activity may lead to the production of reactive oxygen species (ROS) and to subsequent damage to the photosynthetic apparatus [5,6].…”

Anhydrobiosis and programmed cell death in plants: Commonalities and Differences

“…The rate of dissipation is even faster than energy capture process by the active reaction centre. In such scenarios where this photoprotection mechanism is insufficient, a second mechanism may become operational wherein energy dissipation is permitted in the reaction centre itself [51].…”