Climate Change and the Impact of Greenhouse Gasses: CO2 and NO, Friends and Foes of Plant Oxidative Stress

Abstract

Here, we review information on how plants face redox imbalance caused by climate change, and focus on the role of nitric oxide (NO) in this response. Life on Earth is possible thanks to greenhouse effect. Without it, temperature on Earth's surface would be around -19°C, instead of the current average of 14°C. Greenhouse effect is produced by greenhouse gasses (GHG) like water vapor, carbon dioxide (CO₂), methane (CH₄), nitrous oxides (N_xO) and ozone (O₃). GHG have natural and anthropogenic origin. However, increasing GHG provokes extreme climate changes such as floods, droughts and heat, which induce reactive oxygen species (ROS) and oxidative stress in plants. The main sources of ROS in stress conditions are: augmented photorespiration, NADPH oxidase (NOX) activity, β-oxidation of fatty acids and disorders in the electron transport chains of mitochondria and chloroplasts. Plants have developed an antioxidant machinery that includes the activity of ROS detoxifying enzymes [e.g., superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), glutathione peroxidase (GPX), and peroxiredoxin (PRX)], as well as antioxidant molecules such as ascorbic acid (ASC) and glutathione (GSH) that are present in almost all subcellular compartments. CO₂ and NO help to maintain the redox equilibrium. Higher CO₂ concentrations increase the photosynthesis through the CO₂-unsaturated Rubisco activity. But Rubisco photorespiration and NOX activities could also augment ROS production. NO regulate the ROS concentration preserving balance among ROS, GSH, GSNO, and ASC. When ROS are in huge concentration, NO induces transcription and activity of SOD, APX, and CAT. However, when ROS are necessary (e.g., for pathogen resistance), NO may inhibit APX, CAT, and NOX activity by the S-nitrosylation of cysteine residues, favoring cell death. NO also regulates GSH concentration in several ways. NO may react with GSH to form GSNO, the NO cell reservoir and main source of S-nitrosylation. GSNO could be decomposed by the GSNO reductase (GSNOR) to GSSG which, in turn, is reduced to GSH by glutathione reductase (GR). GSNOR may be also inhibited by S-nitrosylation and GR activated by NO. In conclusion, NO plays a central role in the tolerance of plants to climate change.

Keywords: climate change; greenhouse effect; nitric oxide; oxidative stress; plants.

FIGURE 1

Simplified scheme showing greenhouse gasses (GHG) and their effects on plants. GHG (H₂O vapor, clouds, CO₂, CH₄, N₂O, and NO) have both natural and anthropogenic origin, contributing to greenhouse effect. Short-term effects of GHG increase is mainly CO₂ rise, that activates photosynthesis (PS) and inhibits stomatal opening (SO). Long-term effects of GHG increase are extreme climate changes such as floods, droughts, heat. All of them induce the generation of reactive oxygen species (ROS) and oxidative stress in plants. Nitric oxide (NO) could alleviate oxidative stress by scavenging ROS and/or regulating the antioxidant system (AS). GHG and volatile organic compounds (VOC) react in presence of sunlight (E#) to give tropospheric O₃. Although tropospheric O₃ is prejudicial for life, stratospheric O₃ is beneficial, because filters harmful UV-B radiation. The size of arrows are representative of the GHG concentration.

FIGURE 2

Interplay between CO₂ and NO in plant redox physiology: CO₂ enters to the leaves by stomata. Once in mesophyll cells, CO₂ increase photosynthesis (PS) through the CO₂-unsaturated Rubisco activity. When plants are in stress environments, ROS could be augmented by Rubisco-induced photorespiration and NADPH oxidase (NOX) activities. NOX- induced ${\mathrm{O}}_{\mathrm{2}}^{\mathrm{•–}}$, in the apoplast is immediately transformed to H₂O₂ by the superoxide dismutase (SOD). Plasma membrane is permeable to H₂O₂. CO₂ moderates oxidative stress in mesophyll cells by inhibiting both Rubisco photorespiration (PR) and NOX activities. Besides, NO is induced by CO₂ and ROS, alleviating the consequences of oxidative stress by scavenging ROS and activating or inhibiting the antioxidant system (AS). In guard cells, CO₂ increases the expression and activity of OPEN STOMATA 1 (OST1), in both ABA-dependent and independent mechanisms. OST1 activates NOX, producing ROS and consequently NO increase by nitrate reductase (NR), and NOS-like activities. NO prevents ROS increase by direct scavenging, and inhibiting NOX. NO-dependent Ca₂⁺ regulated ion channels induces stomatal closure, modulating O₃ and CO₂ uptake, decreasing evapotranspiration, and rising leaf temperature.

FIGURE 3

Molecules and mechanisms involved in NO-mediated redox balance. H₂O₂ is generated mainly by NOX and SOD as a response to (a)biotic stress. APX and CAT are the main H₂O₂-degrading enzymes. NO is increased by H₂O₂ through the induction of NR/NOS-like activities, and may scavenge ROS or induce both the transcription and activity of SOD, CAT, and APX. In parallel, NO is combined with GSH to form nitrosoglutathione GSNO. GSNO regulates many enzymatic activities by the posttranslational modification of cysteine residues through S-Nitrosylation. NOX and CAT activities are inhibited by S-nitrosylation, whereas APX is either activated or inhibited by S-nitrosylation. NO also inhibits APX by binding to heme group. GSNO is degraded by GSNOR, which could be inhibited by H₂O₂ and S-nitrosylation.NR could be inhibited by S-nitrosylation. GR reduces GSSG to GSH, and it is activated by S-nitrosylation. Ascorbate (ASC) is a cofactor of APX. Reduced ASC is generated by MDHAR and DHAR, using GSH as electron donor. Both enzymes are inhibited by S-nitrosylation. Reactive Nitrogen Species (RNS) may be originated by NO and ${\mathrm{O}}_{\mathrm{2}}^{\mathrm{•–}}$ reaction. SOD regulate RNS dismutating ${\mathrm{O}}_{\mathrm{2}}^{\mathrm{•–}}$. Peroxiredoxins (Prx) reduce both ROS AND RNS. RNS are degraded by PrxIIe, and H₂O₂ by PrxIIF. Both enzymes are inhibited by S-nitrosylation. Red lines: H₂O₂-regulated reactions. Purple lines: NO-regulated reactions. Green lines: GSNO-regulated reactions.