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Shifting Paradigms and Novel Players in Cys- Based Redox Regulation and ROS Signaling in Plants

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Shifting Paradigms and Novel Players in Cys- Based Redox Regulation and ROS Signaling in Plants Biol. Chem. 2021; 402(3): 399–423 Review Andreas J. Meyer*, Anna Dreyer, José M. Ugalde, Elias Feitosa-Araujo, Karl-Josef Dietz* and Markus Schwarzländer* Shifting paradigms and novel players in Cys- based redox regulation and ROS signaling in plants - and where to go next https://doi.org/10.1515/hsz-2020-0291 governance principles of the redox network, (6) gluta- Received August 26, 2020; accepted November 9, 2020; thione peroxidase-like proteins, (7) ferroptosis, (8) oxida- published online November 27, 2020 tive protein folding in the ER for phytohormonal regulation, (9) the apoplast as an unchartered redox fron- Abstract: Cys-based redox regulation was long regarded a tier, (10) redox regulation of respiration, (11) redox transi- major adjustment mechanism of photosynthesis and tions in seed germination and (12) the mitochondria as metabolism in plants, but in the recent years, its scope has potential new players in reductive stress safeguarding. Our broadened to most fundamental processes of plant life. emerging understanding in plants may serve as a blueprint Drivers of the recent surge in new insights into plant redox to scrutinize principles of reactive oxygen and Cys-based regulation have been the availability of the genome-scale redox regulation across organisms. information combined with technological advances such as quantitative redox proteomics and in vivo biosensing. Keywords: apoplast; chloroplast; endoplasmic reticulum; Several unexpected findings have started to shift para- hydrogen peroxide; mitochondrion; redox regulation. digms of redox regulation. Here, we elaborate on a selec- tion of recent advancements, and pinpoint emerging areas and questions of redox biology in plants. We highlight the Introduction significance of (1) proactive H2O2 generation, (2) the chlo- roplast as a unique redox site, (3) specificity in thioredoxin Cys-based redox regulation has claimed a central place in complexity, (4) how to oxidize redox switches, (5) the control of metabolic, developmental and acclimatory processes of plants in recent years. Drivers in under- standing were advancements in technologies and novel *Corresponding authors: Andreas J. Meyer, Chemical Signalling, approaches. In this context, photosynthetic cells serve Institute of Crop Science and Resource Conservation (INRES), both as a biological system with outstanding importance University of Bonn, Friedrich-Ebert-Allee 144, D-53113 Bonn, Germany, for life providing carbon and energy on the one hand, and E-mail: [email protected]. https://orcid.org/0000-0001- as a blueprint to scrutinize principles and dynamics of 8144-4364; Karl-Josef Dietz, Biochemistry and Physiology of Plants, reactive oxygen species and redox regulation on the other Faculty of Biology, W5-134, Bielefeld University, University Street 25, hand. Since evolution has been utilizing the redox regu- D-33501 Bielefeld, Germany, E-mail: karl-josef.dietz@uni- bielefeld.de. https://orcid.org/0000-0003-0311-2182; and Markus latory toolbox in different contexts in different organisms Schwarzländer, Plant Energy Biology, Institute of Plant Biology and depending on their specific lifestyles we expect particular Biotechnology (IBBP), University of Münster, Schlossplatz 8, D-48143 sophistication for a photoautotrophic, sessile organism. At Münster, Germany, E-mail: [email protected]. the same time, we expect the toolbox to be employed under https://orcid.org/0000-0003-0796-8308 the same fundamental biophysical and biochemical con- Anna Dreyer, Biochemistry and Physiology of Plants, Faculty of Biology, W5-134, Bielefeld University, University Street 25, D-33501 straints across biology. In this review, we discuss recent Bielefeld, Germany advancements in understanding the dynamics and the José M. Ugalde, Chemical Signalling, Institute of Crop Science and scope of redox regulation in plants. The article does not Resource Conservation (INRES), University of Bonn, aim to present a comprehensive coverage of redox systems Friedrich-Ebert-Allee 144, D-53113 Bonn, Germany. https://orcid.org/ and target processes. For the sake of focus we deliberately 0000-0002-0601-4302 chose to leave out important aspects, which have also Elias Feitosa-Araujo, Plant Energy Biology, Institute of Plant Biology and Biotechnology (IBBP), University of Münster, Schlossplatz 8, experienced extensive progress, such as protein nitro- D-48143 Münster, Germany. https://orcid.org/0000-0002-2523-2372 sylation, sulfenylation, persulfidation, and H2S signaling. Open Access. © 2020 Andreas J. Meyer et al., published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 International License. 400 A.J. Meyer et al.: Paradigm shifts in redox regulation in plants Rather, we highlight a selection of recent major changes in mechanisms for this positive flavodoxin effect in transgenic thinking and concepts in context of Cys-based redox- and angiosperms, namely (i) their function as efficient electron reactive oxygen species (ROS) signaling. sink particularly when the active ferredoxin pool declines during senescence or under stress, (ii) the stimulation of the antioxidant systems and (iii) maintenance of a balanced Paradigm shift 1: ROS production reduced state of the cell. PET-dependent ROS production comes with a negative takes place under any condition tradeoff under severe stress due to its damaging potential but is an important regulator under conditions of low and − Superoxide (O2 ), hydrogen peroxide (H2O2) and other ROS medium stress, and possibly particularly relevant under are formed both as byproducts of cellular metabolism and fluctuating environmental conditions. An analogous argu- fi − through speci cally evolved generator systems. Several of ment can be made for RET in the mitochondria, where O2 is the underlying cellular processes and chemical mechanisms readily formed at specific sites at the complexes I and III, but are known and have been extensively covered in reviews not others (Huang et al. 2016; Murphy 2009). The fact that (Apel and Hirt 2004; Waszczak et al. 2018). For more than a mitochondrial ROS production has not been ‘fixed’ during quarter of a century, the relevant literature stresses that ROS evolution could either mean that (i) avoiding it is bio- should no longer be considered solely as damaging com- chemically impossible or (ii) that ROS production has pounds but as signaling messengers, e.g., involved in con- adopted an important physiological role and its absence trolling local and global acclimation responses or in would come with a disadvantage that is selected against. triggering cell death programs. Before that paradigm shift, The rate and function of Mehler reaction in the PET of ROS were merely considered markers of severe stress and angiosperms have long been a matter of debate but, more dysfunction. recently, evidence in favor of a suppressed rate of the Currently we are witness to a second major paradigm Mehler reaction with a role in electron transport regulation shift. H2O2 and other ROS are now regarded as essential appears to prevail (Heber 2002). O2 photoreduction is lower under any physiological condition by functioning as vital, in angiosperms than in gymnosperms (Shirao et al. 2013). and readily available, electron sinks to properly adjust the The low rate of O2 reduction is consistent with results in redox state of cellular Cys-based redox systems. French bean from Driever and Baker (2011) who interpreted ROS are products of enzymatic reactions of metabolism, the low rate as indication for function in regulation, rather electron transport chains and specific generator systems. than for function as a major alternative electron sink. While L-2-hydroxyacid oxidases, which include glycolate oxidase the paradigm of ROS generation is still in the process of in photorespiration, and glucose oxidase are examples shifting, the emerging new picture regards ROS production of enzymes, which release stoichiometric H2O2 amounts by PET and RET as required for normal physiology, selected in normal metabolism, usually in peroxisomes (Foyer and for and maintained by evolution, and actively regulated. Noctor 2003; Pan et al. 2020). Some oxidases like polyamine oxidase (PAOs) reside in the apoplast and contribute to bi- otic and abiotic stress acclimation (Pottosin et al. 2014) (see Paradigm shift 2: photosynthesis Paradigm shift 9). makes the chloroplast stroma a Photosynthetic electron transport (PET) and respiratory − electron transport (RET) generate O2 which readily dis- unique ‘redox battle ground’ mutates to O2 and H2O2. Interestingly, evolution of PET in angiosperms is based on ferredoxin as the terminal electron Ever since the discovery of the thioredoxins (TRXs) in the hub, which eases ROS production, while cyanobacteria, chloroplasts (Wolosiuk and Buchanan 1977), they have algae and plant lineages other than angiosperms rely on a retained their significance as a biological hotspot in redox group of Fe- and flavin-dependent electron transmitters that regulation. Their importance is reflected by the number scarcely produce ROS in the Mehler reaction but fully reduce and diversity of TRXs and TRX-like proteins (Geigenberger O2 to H2O. Thus, flavodiiron proteins transfer electrons from et al. 2017), which greatly exceeds the number in non-plant PET to O2 and produce H2O without intermittent release of organisms (see Paradigm shift 3). − O2 or H2O2 (Santana-Sanchez et al. 2019). Flavodoxin- Three key characteristics of photosynthesis make stro- expressing tobacco
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