Oxidative protein folding: state‐of‐the‐art and current avenues of research in plants

Abstract

Contents Summary I. Introduction II. Formation and isomerization of disulfides in the ER and the Golgi apparatus III. The disulfide relay in the mitochondrial intermembrane space: why are plants different? IV. Disulfide bond formation on luminal proteins in thylakoids V. Conclusion Acknowledgements References SUMMARY: Disulfide bonds are post-translational modifications crucial for the structure and function of thousands of proteins. Their formation and isomerization, referred to as oxidative folding, require specific protein machineries found in oxidizing subcellular compartments, namely the endoplasmic reticulum and the associated endomembrane system, the intermembrane space of mitochondria and the thylakoid lumen of chloroplasts. At least one protein component is required for transferring electrons from substrate proteins to an acceptor that is usually molecular oxygen. For oxidation reactions, incoming reduced substrates are oxidized by thiol-oxidoreductase proteins (or domains in case of chimeric proteins), which are usually themselves oxidized by a single thiol oxidase, the enzyme generating disulfide bonds de novo. By contrast, the description of the molecular actors and pathways involved in proofreading and isomerization of misfolded proteins, which require a tightly controlled redox balance, lags behind. Herein we provide a general overview of the knowledge acquired on the systems responsible for oxidative protein folding in photosynthetic organisms, highlighting their particularities compared to other eukaryotes. Current research challenges are discussed including the importance and specificity of these oxidation systems in the context of the existence of reducing systems in the same compartments.

An Arabidopsis berberine bridge enzyme‐like protein specifically oxidizes cellulose oligomers and plays a role in immunity

“…The flavin cofactor itself may contribute to the regulation of the function of these enzymes, through its ability to function as a redox sensor (Becker et al ., ). Whether the important changes in the redox state of the apoplast occurring during the immune response modulate the activity of BBE‐like proteins, by regulating the flavin redox state or the thiol/disulfide balance, which is also crucial for the regulation of the activity (Yi and Khosla, ; Meyer et al ., ) is a key aspect to be investigated. On the other hand, elicitation and pathogen infection upregulate the expression of both OGOXs and CELLOX.…”

Shifting paradigms and novel players in Cys-based redox regulation and ROS signaling in plants - and where to go next

“…Formation of structural disulfides is essential for many ER-resident proteins and for proteins passing the ER on the way to their final destination [reviewed in Meyer et al (2019)]. De novo disulfide formation by ER thiol oxidases (EROs) is followed by transfer of disulfides to nascent proteins through a cascade of thiol-disulfide exchange reactions involving several disulfides in ERO and PDIs.…”

The fluorescent protein sensor roGFP2‐Orp1 monitors in vivo H2O2 and thiol redox integration and elucidates intracellular H2O2 dynamics during elicitor‐induced oxidative burst in Arabidopsis

“…Although it is notoriously difficult to quantify the relative contribution of different mechanisms to total H 2 O 2 production in vivo , specific steps in the photosynthetic and respiratory electron transport chains, peroxisomal carbon metabolism and cell wall peroxidases as well as plasma membrane NADPH oxidases are often assumed to dominate cellular H 2 O 2 production. Yet, other redox active proteins, such as the flavoenzymes involved in central metabolism and oxidative protein folding, are also able to reduce molecular oxygen to H 2 O 2 , and may turn into sources of major H 2 O 2 flux under specific conditions (Meyer et al ., ).…”