Viewing oxidative stress through the lens of oxidative signalling rather than damage

Abstract

Concepts of the roles of reactive oxygen species (ROS) in plants and animals have shifted in recent years from focusing on oxidative damage effects to the current view of ROS as universal signalling metabolites. Rather than having two opposing activities, i.e. damage and signalling, the emerging concept is that all types of oxidative modification/damage are involved in signalling, not least in the induction of repair processes. Examining the multifaceted roles of ROS as crucial cellular signals, we highlight as an example the loss of photosystem II function called photoinhibition, where photoprotection has classically been conflated with oxidative damage.

Keywords: cell signalling; oxidative stress; photoinhibition; photosynthesis; reactive oxygen species.

Figure 1.. Matching supply and demand in photosynthesis.

Light energy drives otherwise thermodynamically unfavourable electron transfer at PSI and PSII to enable the reduction in ferredoxin (F_d) and NADP⁺ in the stroma. Electron transfer is accompanied by the release of protons into the intrathylakoid space during water-splitting at PSII and plastoquinol oxidation at the cytochrome b₆f complex (CBF). The protons are used by the coupling factor to produce ATP which, together with the NADPH generated from electron transport, drives metabolism in the stroma. If the proton concentration inside the thylakoid reaches a certain value, non-photochemical quenching (NPQ) mechanisms are activated to enable energy dissipation as heat. Oxygen oils the wheels of the whole process: the continuous production of ROS at various sites in the electron transport chain serves numerous functions, including contributing to the proton gradient required for ATP generation, redox poising (adjustments of the ratios of reduced to oxidised forms of electron transfer components) and providing information on current status through signalling pathways.

Figure 2.. A typical pulse amplitude-modulated chlorophyll fluorescence induction measurement.

The modulated low intensity measuring light of ∼1 µmol m⁻² s⁻¹ is used to excite chlorophylls of the PSII antenna fluorescence (F_o level). In these conditions, fluorescence is highly quenched by working RCs (RCIIs). Application of a saturating light (10 000 µmol m⁻² s⁻¹) for 1 s causes the closure of all reaction centres for the measuring light so that they stop quenching of the antenna fluorescence and the level rises to F_m. After ∼1 min, a continuous illumination is applied (actinic light) of an intensity of ∼800 µmol m⁻² s⁻¹. This causes gradual quenching of F_m to the F′_m level. This quenching is triggered by the proton gradient and called NPQ. After ∼5 min, the actinic light is turned off and NPQ begins to recover. The recovery that is not complete within 5 min of darkness is termed qI.