Redox Homeostasis and Signaling in a Higher-CO₂World

Abstract

Rising CO2 concentrations and their effects on plant productivity present challenging issues. Effects on the photosynthesis/photorespiration balance and changes in primary metabolism are known, caused by the competitive interaction of CO2 and O2 at the active site of ribulose-1,5-bisphosphate carboxylase/oxygenase. However, impacts on stress resistance are less clear. Reactive oxygen species are key players in biotic and abiotic stress responses, but there is no consensus on whether elevated CO2 constitutes a stress. Although high CO2 increases yield in C3 plants, it can also increase cellular oxidation and activate phytohormone defense pathways. Reduction-oxidation processes play key roles in acclimation to high CO2, with specific enzymes acting in compartment-specific signaling. Traditionally, acclimation to high CO2 has been considered in terms of altered carbon gain, but emerging evidence suggests that CO2 is a signal as well as a substrate. Some CO2 effects on defense are likely mediated independently of primary metabolism. Nonetheless, primary photosynthetic metabolism is highly integrated with defense and stress signaling pathways, meaning that plants will be able to acclimate to the changing environment over the coming decades.

Signaling Toward Reactive Oxygen Species-Scavenging Enzymes in Plants

“…ROS scavenging is performed enzymatic or via non-enzymatic antioxidant defense pathways, which control the regulation of ROS levels through strict compartmentalization (Mignolet-Spruyt et al, 2016;Noctor et al, 2017;Foyer and Noctor, 2020). Non-enzymatic antioxidant defense is mainly mediated by low molecular-weight metabolites such as ascorbate, glutathione, α-tocopherol, carotenoids, and flavonoids (Locato et al, 2017;Smirnoff, 2018;Zechmann, 2018;Muñoz and Munné-Bosch, 2019;Foyer and Noctor, 2020). Superoxide dismutases (SODs), catalases (CATs), ascorbate peroxidases (APXs), dehydroascorbate reductases (DHARs), monodehydroascorbate reductases (MDHARs), and glutathione reductases (GRs) are among the main antioxidant enzyme classes.…”

“…Superoxide dismutases (SODs), catalases (CATs), ascorbate peroxidases (APXs), dehydroascorbate reductases (DHARs), monodehydroascorbate reductases (MDHARs), and glutathione reductases (GRs) are among the main antioxidant enzyme classes. Furthermore, glutathione peroxidases, peroxidases, and thio-, gluta-, and peroxiredoxins are potent ROS scavengers as well (Dietz, 2011;Kang et al, 2019;Foyer and Noctor, 2020). Within this section, we briefly characterize the key enzymatic antioxidants in plants.…”

CO2 Elevation Accelerates Phenology and Alters Carbon/Nitrogen Metabolism vis-à-vis ROS Abundance in Bread Wheat

“…In silico gene expression data (Miyazaki et al, 2004;Li et al, 2006) also indicated that CE up-regulates many genes associated with redox control and thus impairment in ROS balance. Recently, Foyer and Noctor (2020) also concluded that apoplastic ROS signals were increased at high CO 2 , and possibly due to the involvement NADPH oxidases (Cheeseman, 2006;Qui et al, 2008;Mhamdi and Noctor, 2016). Although CE helps in the retention of chlorophyll pigment (Li et al, 2019), it might also lead to production of toxic ROS and RNS (reactive nitrogen species) like nitric oxide (NO) (Adavi and Sathee, 2018;Foyer and Noctor, 2020).…”

Glycolate oxidase-dependent H2O2 production regulates IAA biosynthesis in rice

“…In recent decades, information has become increasingly available indicating that photorespiration can influence various biological processes, e.g., carbon metabolism, energetics, nitrogen assimilation, and respiration [ 29 – 31 ]. Remarkably, photorespiration is a major source for H 2 O 2 in photoautotrophic tissues, thereby making important contributions to cellular redox status and signaling [ 2 , 11 , 30 ]. Reports indicate that H 2 O 2 is closely associated with IAA during plant development, and that IAA can facilitate H 2 O 2 accumulation in the roots of maize, tomato, and Arabidopsis to regulate root growth and gravitropism [ 32 – 34 ], while IAA biosynthesis and signaling were inhibited by both exogenous and endogenous H 2 O 2 in Arabidopsis seedlings [ 35 , 36 ].…”

“…After reaching the four-leaf stage, seedlings were transplanted, either being continuously grown in Kimura B complete nutrient solution in a plant growth chamber with a light cycle of 14 h light/10 h dark (30 °C / 25 °C, respectively) at 600 µmol photons m −2 s −1 on average, relative humidity 60%-80%, or grown in paddy fields under natural conditions. For high concentration CO 2 treatment, pre-germinated rice seeds were cultured in Kimura B complete nutrient solution in a plant growth chamber (Percival E-41HO, USA) supplied with 3500 ppm CO 2 [ 30 , 54 , 55 ].…”