Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited

Abstract

Sunlight, the ultimate energy source for life on our planet, enters the biosphere as a direct consequence of the evolution of photoautotrophy. Photoautotrophs must balance the light energy absorbed and trapped through extremely fast, temperature-insensitive photochemistry with energy consumed through much slower, temperature-dependent biochemistry and metabolism. The attainment of such a balance in cellular energy flow between chloroplasts, mitochondria and the cytosol is called photostasis. Photoautotrophs sense cellular energy imbalances through modulation of excitation pressure which is a measure of the relative redox state of QA, the first stable quinone electron acceptor of photosystem II reaction centers. High excitation pressure constitutes a potential stress condition that can be caused either by exposure to an irradiance that exceeds the capacity of C, N, and S assimilation to utilize the electrons generated from the absorbed energy or by low temperature or any stress that decreases the capacity of the metabolic pathways downstream of photochemistry to utilize photosynthetically generated reductants. The similarities and differences in the phenotypic responses between cyanobacteria, green algae, crop plants, and variegation mutants of Arabidopsis thaliana as a function of cold acclimation and photoacclimation are reconciled in terms of differential responses to excitation pressure and the predisposition of photoautotrophs to maintain photostasis. The various acclimation strategies associated with green algae and cyanobacteria versus winter cereals and A. thaliana are discussed in terms of retrograde regulation and the “grand design of photosynthesis” originally proposed by Arnon (1982).

Plastid Genome Instability Leads to Reactive Oxygen Species Production and Plastid-to-Nucleus Retrograde Signaling in Arabidopsis

“…As a result of its lightharvesting capacity, the chloroplast is directly associated with light absorption and, accordingly, is ideally placed to detect environmental fluctuations (Ruckle et al, 2012). The fluctuating environmental conditions are perceived through several important molecular checkpoints, such as the redox state of the photosynthetic electron transport chain (PET), often measured as the excitation pressure of the PSII, or the concentration of reactive oxygen species (ROS) produced by the PET (Huner et al, 2012).…”

Identification and physiological characterization of two sister lines ofindicarice (Oryza sativaL.) with contrasting levels of cold tolerance

“…In the vegetative stage, one of the major effects is the inhibition of photosynthetic activity through reduced electron transport in the photosystem II (PSII) (Jeong et al 2002). Due to reduced activity of electron transport proteins, the PSII (P680) is overloaded with energy excess, damaging PSII proteins and compromising ATP and NADPH production (Hüner et al 2012). Moreover, as a consequence of excess excitation energy, there is formation of triplet chlorophyll, which reacts with molecular oxygen generating singlet oxygen.…”

Mitochondrial Alternative Oxidase Maintains Respiration and Preserves Photosynthetic Capacity during Moderate Drought in Nicotiana tabacum

“…For example, such imbalances may occur in the chloroplast when the use of ATP and NADPH by the Calvin cycle does not keep pace with the harvesting of light energy (Hüner et al, 2012). This can result in excess excitation energy that can damage photosynthetic components, perhaps through the generation of ROS (Asada, 2006;Noctor et al, 2014).…”