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Climate Change and the Impact of Greenhouse Gasses: CO 2 and NO, Friends and Foes of Plant Oxidative Stress

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 (CO 2 ), methane (CH 4 ), nitrous oxides (N x O) and ozone (O 3 ). 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. CO 2 and NO help to maintain the redox equilibrium. Higher CO 2 concentrations increase the photosynthesis through the CO 2 -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.

Introduction

Life on Earth, as it is, relies on the natural atmospheric greenhouse effect. This is the result of a process in which a planet’s atmosphere traps the sun radiation and warms the planet’s surface.

Greenhouse effect occurs in the troposphere (the lower atmosphere layer), where life and weather occur. In the absence of greenhouse effect, the average temperature on Earth’s surface is estimated around -19°C, instead of the current average of 14°C ( Le Treut et al., 2007 ). Greenhouse effect is produced by greenhouse gasses (GHG). GHG are those gaseous constituents of the atmosphere that absorb and emit radiation in the thermal infrared range ( IPCC, 2014 ). Traces of GHG, both natural and anthropogenic, are present in the troposphere. The most abundant GHG in increasing order of importance are: water vapor, carbon dioxide (CO 2 ), methane (CH 4 ), nitrous oxides (N x O) and ozone (O 3 ) ( Kiehl and Trenberth, 1997 ). GHG percentages vary daily, seasonally, and annually.

GHG Contribute Differentially to Greenhouse Effect

Water vapor.

Water is present in the troposphere both as vapor and clouds. Water vapor was reported by Tyndal in 1861 as the most important gaseous absorber of variations in infrared radiation (cited in Held and Souden, 2000 ). Further accurate calculation estimate that water vapor and clouds are responsible for 49 and 25%, respectively, of the long wave (thermal) absorption ( Schmidt et al., 2010 ). However, atmospheric lifetime of water vapor is short (days) compared to other GHG as CO 2 (years) ( IPCC, 2014 ).

Water vapor concentrations are not directly influenced by anthropogenic activity and vary regionally. However, human activity increases global temperatures and water vapor formation indirectly, amplifying the warming in a process known as water vapor feedback ( Soden et al., 2005 ).

Carbon Dioxide (CO 2 )

Carbon dioxide is responsible for 20% of the thermal absorption ( Schmidt et al., 2010 ).

Natural sources of CO 2 include organic decomposition, ocean release and respiration. Anthropogenic CO 2 sources are derived from activities such as cement manufacturing, deforestation, fossil fuels combustion such as coal, oil and natural gas, etc. Surprisingly, 24% of direct CO 2 emission comes from agriculture, forestry and other land use, and 21% comes from industry ( IPCC, 2014 ).

Atmospheric CO 2 concentrations climbed up dramatically in the past two centuries, rising from around 270 μmol.mol -1 in 1750 to present concentrations higher than 385 μmol.mol -1 ( Mittler and Blumwald, 2010 ; IPCC, 2014 ). Around 50% of cumulative anthropogenic CO 2 emissions between 1750 and 2010 have taken place since the 1970s ( IPCC, 2014 ). It is calculated that the temperature rise produced by high CO 2 concentrations, plus the water positive feedback, would increase by 3–5°C the global mean surface temperature in 2100 ( IPCC, 2014 ).

Methane (CH 4 )

Methane (CH 4 ) is the main atmospheric organic trace gas. CH 4 is the primary component of natural gas, a worldwide fuel source. Significant emissions of CH 4 result from cattle farming and agriculture, but mainly as a consequence of fossil fuel use. Concentrations of CH 4 were multiplied by two since the pre-industrial era. The present worldwide-averaged concentration is of 1.8 μmol.mol -1 ( IPCC, 2014 ).

Although its concentration represents only 0.5% that of CO 2 , concerns arise regarding a jump in CH 4 atmospheric release. Indeed, it is 30 times more powerful than CO 2 as GHG ( IPCC, 2014 ). CH 4 generates O 3 (see below), and along with carbon monoxide (CO), contributes to control the amount of OH in the troposphere ( Wuebbles and Hayhoe, 2002 ).

Nitrous Oxides (NxO)

Nitrous oxide (N 2 O) and nitric oxide (NO) are GHG. During the last century, their global emissions have rised, due mainly to human intervention ( IPCC, 2014 ). The soil emits both N 2 O and NO. N 2 O is a strong GHG, whereas NO contributes indirectly to O 3 synthesis. As GHG, N 2 O is potentially 300 times stronger than CO 2 . Once in the stratosphere, the former catalyzes the elimination of O 3 ( IPCC, 2014 ). In the atmosphere, N 2 O concentrations are climbing up due mainly to microbial activity in nitrogen (N)-rich soils related with agricultural and fertilization practices ( Hall et al., 2008 ).

Anthropogenic emissions (from combustion of fossil fuels) and biogenic emissions from soils are the main sources of NO in the atmosphere ( Medinets et al., 2015 ). In the troposphere, NO quickly oxidizes to nitrogen dioxide (NO 2 ). NO and NO 2 (termed as NO x ) may react with volatile organic compounds (VOCs) and hydroxyl, resulting in organic nitrates and nitric acid, respectively. They access ecosystems through atmospheric deposition that has an impact on the N cycle as a result of acidification or N enrichment ( Pilegaard, 2013 ).

NO Sources and Chemical Reactions in Plants

Two major pathways for NO production have been described in plants: the reductive and the oxidative pathways. The reductive pathway involves the reduction of nitrite to NO by NR under conditions such as acidic pH, anoxia, or an increase in nitrite levels ( Rockel et al., 2002 ; Meyer et al., 2005 ). NR-dependent NO formation has been involved in processes such as stomatal closure, root development, germination and immune responses. In plants, nitrite may also be reduced enzymatically by other molybdenum enzymes such as, xanthine oxidase, aldehyde oxidase, and sulfite oxidase, in animals ( Chamizo-Ampudia et al., 2016 ) or via the electron transport system in mitochondria ( Gupta and Igamberdiev, 2016 ).

The oxidative pathway produces NO through the oxidation of organic compounds such as polyamines, hydroxylamine and arginine. In animals, NOS catalyzes arginine oxidation to citrulline and NO. Many efforts were made to find the arginine-dependent NO formation in plants, as well as of plant NOS ( Frohlich and Durner, 2011 ). The identification of NOS in the green alga Ostreococcus tauri ( Foresi et al., 2010 ) led to high-throughput bioinformatic analysis in plant genomes. This study shows that NOS homologs were not present in over 1,000 genomes of higher plants analyzed, but only in few photosynthetic microorganisms, such as algae and diatoms ( Di Dato et al., 2015 ; Kumar et al., 2015 ; Jeandroz et al., 2016 ). In summary, although an arginine-dependent NO production is found in higher plants, the specific enzyme/s involved in the oxidative pathways remain elusive.

Ozone (O 3 )

Ozone (O 3 ) is mainly found in the stratosphere, but a little amount is generated in the troposphere. Stratospheric ozone (namely the ozone layer) is formed naturally by chemical reactions involving solar ultraviolet (UV) radiation and O 2 . Solar UV radiation breaks one O 2 molecule, producing two oxygen atoms (2 O). Then, each of these highly reactive atoms combines with O 2 to produce an (O 3 ) molecule. Almost 99% of the Sun’s medium-frequency UV light (from about 200 to 315 nm wavelength) is absorbed by the (O 3 ) layer. Otherwise, they could damage exposed life forms near the Earth surface 1 .

The majority of tropospheric O 3 appears when NOx, CO and VOCs, react in the presence of sunlight. However, it was reported that NOx may scavenge O 3 in urban areas ( Gregg et al., 2003 ). This dual interaction between NOx and O 3 is influenced by light, season, temperature and VOC concentration ( Jhun et al., 2015 ).

Besides, the oxidation of CH 4 by OH in the troposphere gives way to formaldehyde (CH 2 O), CO, and O 3 , in the presence of high amounts of NOx 1 .

Tropospheric O 3 is harmful to both plants and animals (including humans). O 3 affects plants in several ways. Stomata are the cells, mostly on the underside of the plant leaves, that allow CO 2 and water to diffuse into the tissue. High concentrations of O 3 cause plants to close their stomata ( McAdam et al., 2017 ), slowing down photosynthesis and plant growth. O 3 may also provoke strong oxidative stress, damaging plant cells ( Vainonen and Kangasjärvi, 2015 ).

Global Climate Change: an Integrative Balance of the Impact on Plants

Anthropogenic activity alters global climate by interfering with the flows of energy through changes in atmospheric gasses composition, more than the actual generation of heat due to energy usage ( Karl and Trenberth, 2003 ). Short-term consequences of GHG increase in plants are mainly associated with the rise in atmospheric CO 2 . Plants respond directly to elevated CO 2 increasing net photosynthesis, and decreasing stomatal opening ( Long et al., 2004 ). To a lesser extent, O 3 uptake by plants may reduce photosynthesis and induce oxidative stress. In the middle and long term, prognostic consensus about climate change signal a rise in CO 2 concentration and temperature on the Earth’s surface, unexpected variations in rainfall, and more recurrent and intense weather conditions, e.g., heat waves, drought and flooding events ( Mittler and Blumwald, 2010 ; IPCC, 2014 ). These brief episodes bring plants beyond their capacity of adaptation; decreasing crop and tree yield ( Ciais et al., 2005 ; Zinta et al., 2014 ).

Here we will not discuss plants capacity of adaptation to novel environmental conditions when considering large scales and long-term periods. Ecosystems are being affected by climate change at all levels (terrestrial, freshwater, and marine), and it was already reported that species are under evolutionary adaptation to human-caused climate change (for a review see Scheffers et al., 2016 ). Migration and plasticity are two biological mechanisms to cope with these changes. Data indicate that each population of a species has limited tolerance to sharp climate variations, and they could migrate to find more favorable environments. Habitat fragmentation limits plant movement, being other big threat for adaptation ( Stockwell et al., 2003 ; Leimu et al., 2010 ). Despite the fact that individual plants are immobile, plant populations move when seeds are dispersed, resulting in differences in the general distribution of the species ( Corlett and Westcott, 2013 ). In this sense, anthropogenic activities also contribute to seed dispersal.

Plasticity is a characteristic related to phenology and phenotype. Phenology is the timing of phases occurrence in the life cycle, and phenotypic plasticity is the range of phenotypes that a single genotype may express depending on its environment ( Nicotra et al., 2010 ). Plasticity is adaptive when the phenotype changes occur in a direction favored by selection in the new environment.

Climate Change and ROS

Reactive Oxygen Species (ROS) are continuously generated by plants under normal conditions. However, they are increased in response to different abiotic stresses. One of the most important effects of climate change-related stresses at the molecular level is the increase of ROS inside the cells ( Farnese et al., 2016 ). Among ROS, the most studied are superoxide anion ( O 2 •– ), H 2 O 2 and the hydroxyl radical (⋅OH - ).

Reactive Oxygen Species cause damage to proteins, lipids and DNA, affecting cell integrity, morphology, physiology, and, consequently, the growth of plants ( Frohnmeyer and Staiger, 2003 ). 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 mitochondrias and chloroplasts ( Apel and Hirt, 2004 ; AbdElgawad et al., 2015 ). Hence, higher plants have evolved in the presence of ROS and have acquired pathways to protect themselves from its toxicity. Plant antioxidant system (AS) 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 (reviewed by Choudhury et al., 2017 ).

In this context, plants have also developed a tight interaction between ROS and NO as a mechanism to reduce the deleterious consequences of these ROS-induced oxidative injuries. NO orchestrates a wide range of mechanisms leading to the preservation of redox homeostasis in plants. Consequently, NO at low concentration is considered a broad-spectrum anti-stress molecule ( Lamattina et al., 2003 ; Tossi et al., 2009 ; Correa-Aragunde et al., 2015 ). Figure ​ Figure1 1 shows the relationship among the different GHG and their impact on plants.

Simplified scheme showing greenhouse gasses (GHG) and their effects on plants. GHG (H 2 O vapor, clouds, CO 2 , CH 4 , N 2 O, and NO) have both natural and anthropogenic origin, contributing to greenhouse effect. Short-term effects of GHG increase is mainly CO 2 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 O 3 . Although tropospheric O 3 is prejudicial for life, stratospheric O 3 is beneficial, because filters harmful UV-B radiation. The size of arrows are representative of the GHG concentration.

CO 2 and NO Contribute to Regulate Redox Homeostasis in Plants

Co 2 increasing: advantages and disadvantages.

Increased CO 2 was suggested to have a “fertilization” effect, because crops would increase their photosynthesis and stomatal conductance in response to elevated CO 2 . This belief was supported by studies performed in greenhouses, laboratory controlled-environment chambers, and transparent field chambers, where emitted CO 2 may be held back and readily controlled ( Drake et al., 1997 ; Markelz et al., 2014 ). However, more realistic results, obtained by Free-Air Concentration Enrichment (FACE) technology, suggest that the fertilization response due to CO 2 increase is probably dependent on genetic and environmental factors, and the duration of the study ( Smith and Dukes, 2013 ). An extensive review of the literature in this field made by Xu et al. (2015) concluded that augmented CO 2 normally increases photosynthesis in C3 species such as rice, soybean and wheat. On the other hand, they pointed out that a negative feedback of photosynthesis could take place in augmented CO 2 , as a result of overload of chemical and reactive generated substrates, leading to an imbalance in the sink:source carbon ratio. Moreover, the energetic cost of carbohydrate exportation increases in elevated CO 2 level.

The most important photosynthetic enzyme is the ribulose-1,5-bisphosphate carboxylase-oxygenase (RuBisCO). Rubisco is located in mesophyll cells of C3 plants, in direct contact with the intercellular air space linked to the atmosphere by epidermal stomatal pores. Photosynthesis increases at high CO 2 , because Rubisco is not CO 2 saturated and CO 2 inhibits the oxygenation reactions and photorespiration ( Long et al., 2006 ). However, long-term high concentration of CO 2 may down regulate Rubisco activity because ribulose-1,5-bisphosphate is not regenerated. Hexokinase (HXK), a sensor of extreme photosynthate, may participate in the down regulation of Rubisco concentration ( Xu et al., 2015 ). Moreover, severe abiotic stresses, such as temperature and drought, may restrain Rubisco carboxylation and foster oxygenation ( Xu et al., 2015 ).

In C4 crops, such as maize and sorghum, the elevated concentration of CO 2 inside the bundle sheath cells could prevent a large increase of Rubisco activity at higher atmospheric CO 2 and, thereby, photosynthetic activity is not augmented. However, at high CO 2 levels, the water status of C4 plants under drought conditions is improved, increasing photosynthesis and biomass accumulation ( Long et al., 2006 ; Mittler and Blumwald, 2010 ). That envisages potential advantages for the C4 species in future climatic change scenarios, particularly in arid and semiarid areas.

In addition, high CO 2 has the benefit of reducing stomatal conductance, decreasing 10% evapotranspiration in both C3 and C4 plants. Simultaneously, the cooling decreased resulting from reduced transpiration causes elevated canopy temperatures of around 0.7°C for most crops. Biomass and yield rise due to high CO 2 in all C3 plants, but not in C4 plants exception made when water is a restraint. Yields of C3 grain crops jump around 19% on average at high CO 2 ( Kimball, 2016 ).

Some reports analyze the contribution of CO 2 in the responses of plants to the combination of multiple stresses. For Arabidopsis thaliana , the combination of heat and drought induces photosynthesis inhibition of 62% under ambient CO 2 , but the drop in photosynthesis is just 40% at high CO 2 . Moreover, the protein oxidation increases significantly during a heat wave and drought, and this effect is repressed by increased CO 2 . Photorespiration is also reduced by high CO 2 ( Zinta et al., 2014 ).

Studying grasses ( Lolium perenne, Poa pratensis ) and legumes ( Medicago lupulina, Lotus corniculatus ) exposed to drought, high temperature and augmented CO 2 , AbdElgawad et al. (2015) demonstrated that drought suppresses plant growth, photosynthesis and stomatal conductance, and promotes in all species the synthesis of osmolytes and antioxidants. Instead, oxidative damage is more markedly observed in legumes than in grasses. In general, warming amplifies drought consequences. In contrast, augmented CO 2 diminishes stress impact. Reduction in photosynthesis and chlorophyll, as a result of drought and elevated temperature, were avoided by high CO 2 in the grasses. Noxious effects of oxidative stress, i.e., lipid peroxidation, are phased down in all species by augmented CO 2 . Normally, a reduced impact of oxidative stress is due to decreased photorespiration and diminished NOX activity. In legumes, a rise in levels of antioxidant molecules (flavonoids and tocopherols) contribute as well to the stress mitigation caused by augmented CO 2 . The authors draw the conclusion that these different responses point at an unequal future impact of climate change on the production of agricultural-scale legumes and grass crops.

Kumari et al. (2015) assessed the impact of various levels of CO 2 , ambient (382 ppm) and augmented (570 ppm), and O 3 , ambient (50 ppb) and augmented (70 ppb) on the potato physiological and biochemical responses ( Solanum tuberosum ). They observed that augmented CO 2 cut down O 3 uptake, enhanced carbon assimilation, and curbed oxidative stress. Elevated CO 2 also mitigated the noxious effect of high O 3 on photosynthesis.

Although some molecular mechanisms underpinning CO 2 actions are unknown, the results presented highlight the importance of CO 2 as a regulator that mitigates the potential climate change-induced deleterious consequences in plants. Recent reports suggest that some CO 2 -associated responses may be mediated by NO.

Du et al. (2016) determined that 800 μmol.mol -1 of CO 2 increased the NO concentration in Arabidopsis leaves, through a mechanism related to nitrate availability. Moreover, NO increase, as a consequence of high CO 2 levels, was reported as a general procedure to improve iron (Fe) nutrition in response to Fe deficiency in tomato roots ( Jin et al., 2009 ).

The gas exchange between the atmosphere and plants is mainly regulated by stomata. But structure and physiology of stomata are also influenced by gasses ( García-Mata and Lamattina, 2013 ). Elevated CO 2 regulate stomatal density and conductance. Moreover, there is increasing evidence that this response is modified by interaction of CO 2 with other environmental factors ( Xu et al., 2016 ; Yan et al., 2017 ). Wang et al. (2015) reported that 800 μmol.mol -1 of CO 2 increases the NO concentration in A. thaliana guard cells, inducing stomatal closure. Both NR and NO synthase (NOS)-like activities are necessary for CO 2 -induced NO accumulation. Comprehensive pharmacological and genetic results obtained in Arabidopsis by Chater et al. (2015) , show that when CO 2 concentration is around 700–1000 ppm, stomatal density and closure are reduced. They also illustrate that those elements necessary for this process are: activation of both ABA biosynthesis genes and the PYR/RCAR ABA receptor, and ROS increase. However, Shi et al. (2015) provide genetic and pharmacological evidence that high CO 2 concentration induces stomatal closure by an ABA-independent mechanism in tomato. They show that 800 μmol.mol -1 of CO 2 increase the expression of the protein kinase OPEN STOMATA 1 (OST1), NOX, and nitrate reductase (NR) genes. They also show that the sequential production of NOX-dependent H 2 O 2 and NR-produced NO are mainly dependent of OST1, and are involved in the CO 2 -induced stomatal closure.

In ABA-dependent mechanisms, ABA is increased by CO 2. The binding of ABA to its receptor (PYR/RCAR) inactivates PP2C, activating OST1. In ABA-independent mechanism, OST1 will be transcriptionally induced by CO 2 . Once activated, OST1 along with Ca 2 + , activates NOX, increasing ROS ( Kim et al., 2010 ). The rise of guard cells ROS enhances NO, cytosolic free Ca 2 + , and pH ( Song et al., 2014 ; Xie et al., 2014 ). ROS and NO release Ca 2 + from internal reservoirs, or influx external Ca 2 + through plasma membrane Ca 2 + in channels. Cytosolic free Ca 2 + inactivate inward K + channels (K + in ) to prevent K + uptake and activate outward K + channels (K + out ) and Cl - (anion) channels (Cl - ) at the plasma membrane ( Blatt, 2000 ; García-Mata et al., 2003 ). Ca 2 + also activates slow anion channel homolog 3 (SLAH3), slow anion channel-associated 1 (SLAC1) and aluminum activated malate transporters (ALMT) ( Roelfsema et al., 2012 ). The consequence of the regulation of cation/anion channels is the net efflux of K + /Cl - /malate and influx of Ca 2 + , making guard cells lose turgor by water outlet, causing stomatal closure.

All together, the results discussed here suggest that CO 2 -induced NO increase is a common plant physiological response to oxidative stresses. Figure ​ Figure2 2 shows the importance of CO 2 and NO in these processes.

Interplay between CO 2 and NO in plant redox physiology: CO 2 enters to the leaves by stomata. Once in mesophyll cells, CO 2 increase photosynthesis (PS) through the CO 2 -unsaturated Rubisco activity. When plants are in stress environments, ROS could be augmented by Rubisco-induced photorespiration and NADPH oxidase (NOX) activities. NOX- induced O 2 •– , in the apoplast is immediately transformed to H 2 O 2 by the superoxide dismutase (SOD). Plasma membrane is permeable to H 2 O 2 . CO 2 moderates oxidative stress in mesophyll cells by inhibiting both Rubisco photorespiration (PR) and NOX activities. Besides, NO is induced by CO 2 and ROS, alleviating the consequences of oxidative stress by scavenging ROS and activating or inhibiting the antioxidant system (AS). In guard cells, CO 2 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 Ca 2 + regulated ion channels induces stomatal closure, modulating O 3 and CO 2 uptake, decreasing evapotranspiration, and rising leaf temperature.

Abiotic Stress, ROS Generation, and Redox Balance: The Key Role of NO

Reactive oxygen species are generated in apoplast, plasma membrane, chloroplasts, mitochondria, and peroxisomes ( Farnese et al., 2016 ). It was proposed that each stress produces its own “ROS signature” ( Choudhury et al., 2017 ). For instance, drought may reduce the activity of Rubisco, decreasing CO 2 fixation and NADP+ regeneration by the Calvin cycle. As a consequence, chloroplast electron transport is altered, generating ROS by electron leakage to O 2 ( Carvalho, 2008 ). In drought stress, ROS increase is produced by NOX activity ( Farnese et al., 2016 ). In flooding, ROS generation is an ethylene-promoted process that involves calcium (Ca 2+ ) flux, and NOX activity ( Voesenek and Bailey-Serres, 2015 ).

In heat stress, a NOX-dependent transient ROS rise is an early event ( Königshofer et al., 2008 ). Then, endogenous ROS are sensed through histidine kinases, and an Arabidopsis heat stress factor (HsfA4a) appears to sense exogenous ROS. As a result, the MAPK signal pathway is activated ( Qu et al., 2013 ). Moreover, functional decrease in photosynthetic light reaction induces ROS concentration by high electron leakage from the thylakoid membrane ( Hasanuzzaman et al., 2013 ). In this process, O 2 is the acceptor, generating O 2 •– .

Thus, individual stresses or their different combinations may produce particular “ROS signatures.” Besides their deleterious effects, ROS are recognized as a signal in the plant reaction to biotic and abiotic stressors. ROS may induce programed cell death (PCD) to avoid pathogen spread ( Mur et al., 2008 ), trigger a systemic defense response signal ( Dubiella et al., 2013 ), or avoid the chloroplast antenna overloading by electrons divert ( Choudhury et al., 2017 ).

Whatever the origin and function, ROS concentration must be adequately regulated to avoid excessive concentration and consequent cellular damages. Depending on NO and ROS concentrations, NO has the dual capacity to activate or inhibit the ROS production, and is a key molecule for keeping cellular redox homeostasis under control ( Beligni and Lamattina, 1999a ; Correa-Aragunde et al., 2015 ). NO has a direct ROS-scavenging activity because it holds an unpaired electron, reaching elevated reactivity with O 2 , O 2 •– , and redox active metals. NO can mitigate OH formation by scavenging either Fe or O 2 •– ( Lamattina et al., 2003 ). However, NO reacting with ROS (mainly O 2 •– ) may generate reactive nitrogen species (RNS). An excess of RNS originates a nitrosative stress ( Corpas et al., 2011 ). To avoid the toxicity of nitrosative stress, NO is stored as GSNO in the cell.

GSH as a Redox Buffer. GSNO as NO Reservoir. SNO and S-Nitrosylation

Glutathione (GSH) is a small peptide with the sequence γ-l-glutamyl-l-cysteinyl-glycine that has a cell redox homeostatic impact in most plant tissues. It is a soluble small thiol considered a non-enzymatic antioxidant. It exists in the reduced (GSH) or oxidized state (GSSG), in which two GSH molecules are joined by a disulfide bond ( Rouhier et al., 2008 ). GSH alleviates oxidative damages in plants generated by abiotic stresses, including salinity, drought, higher, low temperature, and heavy metals. GSH is precursor of phytochelatins, polymers that chelate toxic metals and transport them to the vacuole ( Grill et al., 1989 ). Studies shown that GSH contributes to tolerate nickel, cadmium, zinc, mercury, aluminum and arsenate heavy metals in plants ( Asgher et al., 2017 ). Moreover, GSH has a role in the detoxification of ROS both directly, interacting with them, or indirectly, participating of enzymatic pathways. GSH is involved in glutathionylation, a posttranslational modification that causes a mixed disulfide bond between a Cys residue and GSH.

GSH can be oxidized to GSSG by H 2 O 2 and can react with NO to form the nitrosoglutathione (GSNO) derivative. GSNO is an intracellular NO reservoir. It is also a vehicle of NO throughout the cell and organs, spreading NO biological function. GSNO is the largest low-molecular-mass S-nitrosothiol (SNO) in plant cells ( Corpas et al., 2013 ). GSNO metabolism and its reaction with other molecules involve S-nitrosylation and S-transnitrosation which consist of the binding of a NO molecule to a cysteine residue in proteins. Thioredoxin produces protein denitrosylation ( Correa-Aragunde et al., 2013 ). GSNO could be decomposed by the GSNO reductase (GSNOR) to GSSG which, in turn, is reduced to GSH by glutathione reductase (GR).

Glutathione also participates in the GSH/ASC cycle, a series of enzymatic reactions that degrade H 2 O 2 . APX degrades H 2 O 2 using ASC, the other major antioxidant in plants, as cofactor. The oxidized ASC is reduced by monodehydroascorbate reductase (MDHAR) in an NAD(P)H-dependent manner and by dehydroascorbate reductase (DHAR) employing GSH as electron donor. The resulting GSSG is reduced in turn to GSH by GR ( Foyer and Noctor, 2011 ).

Different Effects of NO in the Regulation of Antioxidant Enzymes

The application of NO donors alleviates oxidative stress in plants challenged to abiotic and/or biotic stresses ( Laxalt et al., 1997 ; Beligni and Lamattina, 1999b , 2002 ; Shi et al., 2007 ; Xue et al., 2007 ; Leitner et al., 2009 ).

Besides the direct ROS-scavenging activity of NO, its beneficial effect is exerted by the regulation of the antioxidant enzymes activity that controls toxic levels of ROS and RNS ( Uchida et al., 2002 ; Shi et al., 2005 ; Song et al., 2006 ; Romero-Puertas et al., 2007 ; Bai et al., 2011 ). NO can modulate cell redox balance in plants through the regulation of gene expression, posttranslational modification or by its binding to the heme prosthetic group of some antioxidant enzymes.

SOD catalyzes the dismutation of stress-generated O 2 •– in one of two less harmful species: either molecular oxygen (O 2 ) or hydrogen peroxide (H 2 O 2 ). APX and CAT are the most important enzymes degrading H 2 O 2 in plants. They transform H 2 O 2 to H 2 O and O 2 . APX isoforms are primarily found in the cytosol and chloroplasts, while the CAT isoforms are found in peroxisomes. APX has strong affinity for H 2 O 2 and uses ASC as an electron donor. In contrast, CAT removes H 2 O 2 generated in the peroxisomal respiratory pathway without the need to reduce power. Even though CAT affinity for H 2 O 2 is low, its elevated rate of reaction offers an effective way to detoxify H 2 O 2 inside the cell. PRX may reduce both hydroperoxide and peroxynitrite.

Many reports on different plant species demonstrate that NO induces the transcription and activity of antioxidative enzymes in response to oxidative stress. The tolerance to drought and salt-induced oxidative stress in tobacco is related to the ABA-triggered production of H 2 O 2 and NO. In turn, they induce transcripts and activities of SOD, CAT, APX, and GR ( Zhang et al., 2009 ). UV-B-produced oxidative stress in Glycine max was alleviated by NO donors, which induced transcription and activities of SOD, CAT, and APX ( Santa-Cruz et al., 2014 ). Furthermore, in bean leaves, SOD, CAT, and APX activities are increased by NO donors, and protected from the oxidative stress generated by UV-B irradiation ( Shi et al., 2005 ). Drought tolerance in bermudagrass is improved by ABA-dependent SOD and CAT activities. This effect is regulated by H 2 O 2 and NO, NO acting downstream H 2 O 2 ( Lu et al., 2009 ).

Several antioxidant enzymes have been identified as target of S-nitrosylation, resulting in a change of their biological activity ( Romero-Puertas et al., 2008 ; Bai et al., 2011 ; Fares et al., 2011 ). For instance, NO reinforces recalcitrant seed desiccation tolerance in Antiaris toxicaria by activating the ascorbate-glutathione cycle through S-nitrosylation to control H 2 O 2 accumulation. Desiccation treatment reduced the level of S-nitrosylated APX, GR, and DHAR proteins. Instead, NO gas exposure activated them by S-nitrosylation ( Bai et al., 2011 ). Furthermore, APX was S-nitrosylated at Cys32 during saline stress and biotic stress, enhancing its enzymatic activity ( Begara-Morales et al., 2014 ; Yang et al., 2015 ). In addition, auxin-induced denitrosylation of cytosolic APX provoked inhibition of its activity, followed by an increase of H 2 O 2 concentration and the consequent lateral root formation in Arabidopsis ( Correa-Aragunde et al., 2013 ). Moreover, an inhibitory impact of S-nitrosylation on APX activity was also reported during programmed cell death in Arabidopsis ( de Pinto et al., 2013 ). CAT was identified to be S-nitrosylated in a proteomic study of isolated peroxisomes ( Ortega-Galisteo et al., 2012 ). A decrease of S-nitrosylated CAT under Cd treatment was reported. In addition, in vitro experiments demonstrated a reversible inhibitory effect of APX and CAT activities by NO binding to the Fe of the heme cofactor ( Brown, 1995 ; Clark et al., 2000 ). In addition, NOXs have been involved in plant defense, development, hormone biosynthesis and signaling ( Marino et al., 2012 ). Whereas S-nitrosylation did not affect SOD activities, nitration inhibited Mn-SOD1, Fe-SOD3, and CuZn-SOD3 activity to different degrees ( Holzmeister et al., 2015 ). SOD isoforms could also regulate endogenous NO availability by competing for the common substrate, O 2 •– , and it was demonstrated that bovine SOD may release NO from GSNO ( Singh et al., 1999 ). When GSNO is decomposed by GSNOR, it produces GSSG. GSNOR is also regulated by NO. Frungillo et al. (2014) demonstrated that NO-derived from nitrate assimilation in Arabidopsis inhibited GSNOR1 by S-nitrosylation, preventing GSNO degradation. They proposed that (S)NO controls its own generation and scavenging by modulating nitrate assimilation and GSNOR1 activity. It was also shown that chilling treatment in poplar increased S-nitrosylation of NR, along with a significant decrease of its activity ( Cheng et al., 2015 ).

The dual activity of Prx, suggests a role for this enzyme both in ROS and RNS regulation. S-nitrosylation of Arabidopsis PrxIIE inhibits its peroxynitrite activity, increasing peroxynitrite-mediated tyrosine nitration ( Romero-Puertas et al., 2007 ). Pea mitochondrial PrxIIF was S-nitrosylated under salt stress, and its peroxidase activity was reduced by 5 mM GSNO ( Camejo et al., 2013 ).

An interesting study demonstrated that NO controls hypersensitive response (HR) through S-nitrosylation of NOX, inhibiting ROS synthesis. This triggers a feedback loop limiting HR ( Yun et al., 2011 ).

Other proteins related to abiotic stress response are regulated by S-nitrosylation (For a review see Fancy et al., 2017 ).

Figure ​ Figure3 3 is a simplified diagram that illustrates the main oxidative and nitrosative effects that modulate the activities of key cell components, thus maintaining cell redox balance. Note the feedback and positive-negative regulatory processes occurring in the main pathways. They involve posttranslational modifications that activate and inhibit the components involved in cell antioxidant system.

Molecules and mechanisms involved in NO-mediated redox balance. H 2 O 2 is generated mainly by NOX and SOD as a response to (a)biotic stress. APX and CAT are the main H 2 O 2 -degrading enzymes. NO is increased by H 2 O 2 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 H 2 O 2 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 O 2 •– reaction. SOD regulate RNS dismutating O 2 •– . Peroxiredoxins (Prx) reduce both ROS AND RNS. RNS are degraded by PrxIIe, and H 2 O 2 by PrxIIF. Both enzymes are inhibited by S-nitrosylation. Red lines: H 2 O 2 -regulated reactions. Purple lines: NO-regulated reactions. Green lines: GSNO-regulated reactions.

Conclusions and Perspectives

The accelerating rate of climate change, together with habitat fragmentation caused by human activity, are part of the selective pressures building a new Earth’s landscape.

Climate change is a multidimensional and simultaneous variation in duration, frequency and intensity of parameters like temperature and precipitation, altering the seasons and life on the Earth. In this scenario, plant species with increased adaptive plasticity will be better equipped to tolerate changes in the frequency of extreme weather events. GHG are one of the forces driving climate change. However, CO 2 and NO may contribute to maintaining the cell redox homeostasis, regulating the amount of ROS, GSH, GSNO, and SNO.

In this manuscript, we summarize the available evidence supporting the presence of broad spectrum anti-stress molecules, as NO in plants, for coping with unprecedented changes in environmental conditions. Future research should focus in better understanding the influence of GHG on plant physiology.

Author Contributions

RC conceived the project and wrote the manuscript. MN drew figures and collaborated in writing the manuscript. NC-A and LL supervised and complemented the drafting. All the persons entitled to authorship have been named and have approved the final version of the submitted manuscript.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The reviewer MCR-P and handling Editor declared their shared affiliation.

Acknowledgments

We thank ANPCYT for MN fellowship. We also thank Marta Terrazo for helping with the language revision of the manuscript.

Funding. This work was supported by grants from the Consejo Nacional de Investigaciones Cientificas y Tecnicas, the Agencia Nacional de Promoción Científica y Tecnológica, and the Universidad Nacional de Mar del Plata, Argentina. NC-A, LL, and RC are permanent members of the Scientific Research career of CONICET. MN is doctoral fellow of the ANPCYT.

1 https://ozonewatch.gsfc.nasa.gov/facts/ozone.html

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REVIEW article

Climate change and the impact of greenhouse gasses: co 2 and no, friends and foes of plant oxidative stress.

• Instituto de Investigaciones Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata-Consejo Nacional de Investigaciones Científicas y Técnicas, Mar del Plata, Argentina

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 (CO 2 ), methane (CH 4 ), nitrous oxides (N x O) and ozone (O 3 ). 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. CO 2 and NO help to maintain the redox equilibrium. Higher CO 2 concentrations increase the photosynthesis through the CO 2 -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.

Introduction

Life on Earth, as it is, relies on the natural atmospheric greenhouse effect. This is the result of a process in which a planet’s atmosphere traps the sun radiation and warms the planet’s surface.

Greenhouse effect occurs in the troposphere (the lower atmosphere layer), where life and weather occur. In the absence of greenhouse effect, the average temperature on Earth’s surface is estimated around -19°C, instead of the current average of 14°C ( Le Treut et al., 2007 ). Greenhouse effect is produced by greenhouse gasses (GHG). GHG are those gaseous constituents of the atmosphere that absorb and emit radiation in the thermal infrared range ( IPCC, 2014 ). Traces of GHG, both natural and anthropogenic, are present in the troposphere. The most abundant GHG in increasing order of importance are: water vapor, carbon dioxide (CO 2 ), methane (CH 4 ), nitrous oxides (N x O) and ozone (O 3 ) ( Kiehl and Trenberth, 1997 ). GHG percentages vary daily, seasonally, and annually.

GHG Contribute Differentially to Greenhouse Effect

Water vapor.

Water is present in the troposphere both as vapor and clouds. Water vapor was reported by Tyndal in 1861 as the most important gaseous absorber of variations in infrared radiation (cited in Held and Souden, 2000 ). Further accurate calculation estimate that water vapor and clouds are responsible for 49 and 25%, respectively, of the long wave (thermal) absorption ( Schmidt et al., 2010 ). However, atmospheric lifetime of water vapor is short (days) compared to other GHG as CO 2 (years) ( IPCC, 2014 ).

Water vapor concentrations are not directly influenced by anthropogenic activity and vary regionally. However, human activity increases global temperatures and water vapor formation indirectly, amplifying the warming in a process known as water vapor feedback ( Soden et al., 2005 ).

Carbon Dioxide (CO 2 )

Carbon dioxide is responsible for 20% of the thermal absorption ( Schmidt et al., 2010 ).

Natural sources of CO 2 include organic decomposition, ocean release and respiration. Anthropogenic CO 2 sources are derived from activities such as cement manufacturing, deforestation, fossil fuels combustion such as coal, oil and natural gas, etc. Surprisingly, 24% of direct CO 2 emission comes from agriculture, forestry and other land use, and 21% comes from industry ( IPCC, 2014 ).

Atmospheric CO 2 concentrations climbed up dramatically in the past two centuries, rising from around 270 μmol.mol -1 in 1750 to present concentrations higher than 385 μmol.mol -1 ( Mittler and Blumwald, 2010 ; IPCC, 2014 ). Around 50% of cumulative anthropogenic CO 2 emissions between 1750 and 2010 have taken place since the 1970s ( IPCC, 2014 ). It is calculated that the temperature rise produced by high CO 2 concentrations, plus the water positive feedback, would increase by 3–5°C the global mean surface temperature in 2100 ( IPCC, 2014 ).

Methane (CH 4 )

Methane (CH 4 ) is the main atmospheric organic trace gas. CH 4 is the primary component of natural gas, a worldwide fuel source. Significant emissions of CH 4 result from cattle farming and agriculture, but mainly as a consequence of fossil fuel use. Concentrations of CH 4 were multiplied by two since the pre-industrial era. The present worldwide-averaged concentration is of 1.8 μmol.mol -1 ( IPCC, 2014 ).

Although its concentration represents only 0.5% that of CO 2 , concerns arise regarding a jump in CH 4 atmospheric release. Indeed, it is 30 times more powerful than CO 2 as GHG ( IPCC, 2014 ). CH 4 generates O 3 (see below), and along with carbon monoxide (CO), contributes to control the amount of OH in the troposphere ( Wuebbles and Hayhoe, 2002 ).

Nitrous Oxides (NxO)

Nitrous oxide (N 2 O) and nitric oxide (NO) are GHG. During the last century, their global emissions have rised, due mainly to human intervention ( IPCC, 2014 ). The soil emits both N 2 O and NO. N 2 O is a strong GHG, whereas NO contributes indirectly to O 3 synthesis. As GHG, N 2 O is potentially 300 times stronger than CO 2 . Once in the stratosphere, the former catalyzes the elimination of O 3 ( IPCC, 2014 ). In the atmosphere, N 2 O concentrations are climbing up due mainly to microbial activity in nitrogen (N)-rich soils related with agricultural and fertilization practices ( Hall et al., 2008 ).

Anthropogenic emissions (from combustion of fossil fuels) and biogenic emissions from soils are the main sources of NO in the atmosphere ( Medinets et al., 2015 ). In the troposphere, NO quickly oxidizes to nitrogen dioxide (NO 2 ). NO and NO 2 (termed as NO x ) may react with volatile organic compounds (VOCs) and hydroxyl, resulting in organic nitrates and nitric acid, respectively. They access ecosystems through atmospheric deposition that has an impact on the N cycle as a result of acidification or N enrichment ( Pilegaard, 2013 ).

NO Sources and Chemical Reactions in Plants

Two major pathways for NO production have been described in plants: the reductive and the oxidative pathways. The reductive pathway involves the reduction of nitrite to NO by NR under conditions such as acidic pH, anoxia, or an increase in nitrite levels ( Rockel et al., 2002 ; Meyer et al., 2005 ). NR-dependent NO formation has been involved in processes such as stomatal closure, root development, germination and immune responses. In plants, nitrite may also be reduced enzymatically by other molybdenum enzymes such as, xanthine oxidase, aldehyde oxidase, and sulfite oxidase, in animals ( Chamizo-Ampudia et al., 2016 ) or via the electron transport system in mitochondria ( Gupta and Igamberdiev, 2016 ).

The oxidative pathway produces NO through the oxidation of organic compounds such as polyamines, hydroxylamine and arginine. In animals, NOS catalyzes arginine oxidation to citrulline and NO. Many efforts were made to find the arginine-dependent NO formation in plants, as well as of plant NOS ( Frohlich and Durner, 2011 ). The identification of NOS in the green alga Ostreococcus tauri ( Foresi et al., 2010 ) led to high-throughput bioinformatic analysis in plant genomes. This study shows that NOS homologs were not present in over 1,000 genomes of higher plants analyzed, but only in few photosynthetic microorganisms, such as algae and diatoms ( Di Dato et al., 2015 ; Kumar et al., 2015 ; Jeandroz et al., 2016 ). In summary, although an arginine-dependent NO production is found in higher plants, the specific enzyme/s involved in the oxidative pathways remain elusive.

Ozone (O 3 )

Ozone (O 3 ) is mainly found in the stratosphere, but a little amount is generated in the troposphere. Stratospheric ozone (namely the ozone layer) is formed naturally by chemical reactions involving solar ultraviolet (UV) radiation and O 2 . Solar UV radiation breaks one O 2 molecule, producing two oxygen atoms (2 O). Then, each of these highly reactive atoms combines with O 2 to produce an (O 3 ) molecule. Almost 99% of the Sun’s medium-frequency UV light (from about 200 to 315 nm wavelength) is absorbed by the (O 3 ) layer. Otherwise, they could damage exposed life forms near the Earth surface 1 .

The majority of tropospheric O 3 appears when NOx, CO and VOCs, react in the presence of sunlight. However, it was reported that NOx may scavenge O 3 in urban areas ( Gregg et al., 2003 ). This dual interaction between NOx and O 3 is influenced by light, season, temperature and VOC concentration ( Jhun et al., 2015 ).

Besides, the oxidation of CH 4 by OH in the troposphere gives way to formaldehyde (CH 2 O), CO, and O 3 , in the presence of high amounts of NOx 1 .

Tropospheric O 3 is harmful to both plants and animals (including humans). O 3 affects plants in several ways. Stomata are the cells, mostly on the underside of the plant leaves, that allow CO 2 and water to diffuse into the tissue. High concentrations of O 3 cause plants to close their stomata ( McAdam et al., 2017 ), slowing down photosynthesis and plant growth. O 3 may also provoke strong oxidative stress, damaging plant cells ( Vainonen and Kangasjärvi, 2015 ).

Global Climate Change: an Integrative Balance of the Impact on Plants

Anthropogenic activity alters global climate by interfering with the flows of energy through changes in atmospheric gasses composition, more than the actual generation of heat due to energy usage ( Karl and Trenberth, 2003 ). Short-term consequences of GHG increase in plants are mainly associated with the rise in atmospheric CO 2 . Plants respond directly to elevated CO 2 increasing net photosynthesis, and decreasing stomatal opening ( Long et al., 2004 ). To a lesser extent, O 3 uptake by plants may reduce photosynthesis and induce oxidative stress. In the middle and long term, prognostic consensus about climate change signal a rise in CO 2 concentration and temperature on the Earth’s surface, unexpected variations in rainfall, and more recurrent and intense weather conditions, e.g., heat waves, drought and flooding events ( Mittler and Blumwald, 2010 ; IPCC, 2014 ). These brief episodes bring plants beyond their capacity of adaptation; decreasing crop and tree yield ( Ciais et al., 2005 ; Zinta et al., 2014 ).

Here we will not discuss plants capacity of adaptation to novel environmental conditions when considering large scales and long-term periods. Ecosystems are being affected by climate change at all levels (terrestrial, freshwater, and marine), and it was already reported that species are under evolutionary adaptation to human-caused climate change (for a review see Scheffers et al., 2016 ). Migration and plasticity are two biological mechanisms to cope with these changes. Data indicate that each population of a species has limited tolerance to sharp climate variations, and they could migrate to find more favorable environments. Habitat fragmentation limits plant movement, being other big threat for adaptation ( Stockwell et al., 2003 ; Leimu et al., 2010 ). Despite the fact that individual plants are immobile, plant populations move when seeds are dispersed, resulting in differences in the general distribution of the species ( Corlett and Westcott, 2013 ). In this sense, anthropogenic activities also contribute to seed dispersal.

Plasticity is a characteristic related to phenology and phenotype. Phenology is the timing of phases occurrence in the life cycle, and phenotypic plasticity is the range of phenotypes that a single genotype may express depending on its environment ( Nicotra et al., 2010 ). Plasticity is adaptive when the phenotype changes occur in a direction favored by selection in the new environment.

Climate Change and ROS

Reactive Oxygen Species (ROS) are continuously generated by plants under normal conditions. However, they are increased in response to different abiotic stresses. One of the most important effects of climate change-related stresses at the molecular level is the increase of ROS inside the cells ( Farnese et al., 2016 ). Among ROS, the most studied are superoxide anion ( O 2 •– ), H 2 O 2 and the hydroxyl radical (⋅OH - ).

Reactive Oxygen Species cause damage to proteins, lipids and DNA, affecting cell integrity, morphology, physiology, and, consequently, the growth of plants ( Frohnmeyer and Staiger, 2003 ). 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 mitochondrias and chloroplasts ( Apel and Hirt, 2004 ; AbdElgawad et al., 2015 ). Hence, higher plants have evolved in the presence of ROS and have acquired pathways to protect themselves from its toxicity. Plant antioxidant system (AS) 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 (reviewed by Choudhury et al., 2017 ).

In this context, plants have also developed a tight interaction between ROS and NO as a mechanism to reduce the deleterious consequences of these ROS-induced oxidative injuries. NO orchestrates a wide range of mechanisms leading to the preservation of redox homeostasis in plants. Consequently, NO at low concentration is considered a broad-spectrum anti-stress molecule ( Lamattina et al., 2003 ; Tossi et al., 2009 ; Correa-Aragunde et al., 2015 ). Figure 1 shows the relationship among the different GHG and their impact on plants.

FIGURE 1. Simplified scheme showing greenhouse gasses (GHG) and their effects on plants. GHG (H 2 O vapor, clouds, CO 2 , CH 4 , N 2 O, and NO) have both natural and anthropogenic origin, contributing to greenhouse effect. Short-term effects of GHG increase is mainly CO 2 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 O 3 . Although tropospheric O 3 is prejudicial for life, stratospheric O 3 is beneficial, because filters harmful UV-B radiation. The size of arrows are representative of the GHG concentration.

CO 2 and NO Contribute to Regulate Redox Homeostasis in Plants

Co 2 increasing: advantages and disadvantages.

Increased CO 2 was suggested to have a “fertilization” effect, because crops would increase their photosynthesis and stomatal conductance in response to elevated CO 2 . This belief was supported by studies performed in greenhouses, laboratory controlled-environment chambers, and transparent field chambers, where emitted CO 2 may be held back and readily controlled ( Drake et al., 1997 ; Markelz et al., 2014 ). However, more realistic results, obtained by Free-Air Concentration Enrichment (FACE) technology, suggest that the fertilization response due to CO 2 increase is probably dependent on genetic and environmental factors, and the duration of the study ( Smith and Dukes, 2013 ). An extensive review of the literature in this field made by Xu et al. (2015) concluded that augmented CO 2 normally increases photosynthesis in C3 species such as rice, soybean and wheat. On the other hand, they pointed out that a negative feedback of photosynthesis could take place in augmented CO 2 , as a result of overload of chemical and reactive generated substrates, leading to an imbalance in the sink:source carbon ratio. Moreover, the energetic cost of carbohydrate exportation increases in elevated CO 2 level.

The most important photosynthetic enzyme is the ribulose-1,5-bisphosphate carboxylase-oxygenase (RuBisCO). Rubisco is located in mesophyll cells of C3 plants, in direct contact with the intercellular air space linked to the atmosphere by epidermal stomatal pores. Photosynthesis increases at high CO 2 , because Rubisco is not CO 2 saturated and CO 2 inhibits the oxygenation reactions and photorespiration ( Long et al., 2006 ). However, long-term high concentration of CO 2 may down regulate Rubisco activity because ribulose-1,5-bisphosphate is not regenerated. Hexokinase (HXK), a sensor of extreme photosynthate, may participate in the down regulation of Rubisco concentration ( Xu et al., 2015 ). Moreover, severe abiotic stresses, such as temperature and drought, may restrain Rubisco carboxylation and foster oxygenation ( Xu et al., 2015 ).

In C4 crops, such as maize and sorghum, the elevated concentration of CO 2 inside the bundle sheath cells could prevent a large increase of Rubisco activity at higher atmospheric CO 2 and, thereby, photosynthetic activity is not augmented. However, at high CO 2 levels, the water status of C4 plants under drought conditions is improved, increasing photosynthesis and biomass accumulation ( Long et al., 2006 ; Mittler and Blumwald, 2010 ). That envisages potential advantages for the C4 species in future climatic change scenarios, particularly in arid and semiarid areas.

In addition, high CO 2 has the benefit of reducing stomatal conductance, decreasing 10% evapotranspiration in both C3 and C4 plants. Simultaneously, the cooling decreased resulting from reduced transpiration causes elevated canopy temperatures of around 0.7°C for most crops. Biomass and yield rise due to high CO 2 in all C3 plants, but not in C4 plants exception made when water is a restraint. Yields of C3 grain crops jump around 19% on average at high CO 2 ( Kimball, 2016 ).

Some reports analyze the contribution of CO 2 in the responses of plants to the combination of multiple stresses. For Arabidopsis thaliana , the combination of heat and drought induces photosynthesis inhibition of 62% under ambient CO 2 , but the drop in photosynthesis is just 40% at high CO 2 . Moreover, the protein oxidation increases significantly during a heat wave and drought, and this effect is repressed by increased CO 2 . Photorespiration is also reduced by high CO 2 ( Zinta et al., 2014 ).

Studying grasses ( Lolium perenne, Poa pratensis ) and legumes ( Medicago lupulina, Lotus corniculatus ) exposed to drought, high temperature and augmented CO 2 , AbdElgawad et al. (2015) demonstrated that drought suppresses plant growth, photosynthesis and stomatal conductance, and promotes in all species the synthesis of osmolytes and antioxidants. Instead, oxidative damage is more markedly observed in legumes than in grasses. In general, warming amplifies drought consequences. In contrast, augmented CO 2 diminishes stress impact. Reduction in photosynthesis and chlorophyll, as a result of drought and elevated temperature, were avoided by high CO 2 in the grasses. Noxious effects of oxidative stress, i.e., lipid peroxidation, are phased down in all species by augmented CO 2 . Normally, a reduced impact of oxidative stress is due to decreased photorespiration and diminished NOX activity. In legumes, a rise in levels of antioxidant molecules (flavonoids and tocopherols) contribute as well to the stress mitigation caused by augmented CO 2 . The authors draw the conclusion that these different responses point at an unequal future impact of climate change on the production of agricultural-scale legumes and grass crops.

Kumari et al. (2015) assessed the impact of various levels of CO 2 , ambient (382 ppm) and augmented (570 ppm), and O 3 , ambient (50 ppb) and augmented (70 ppb) on the potato physiological and biochemical responses ( Solanum tuberosum ). They observed that augmented CO 2 cut down O 3 uptake, enhanced carbon assimilation, and curbed oxidative stress. Elevated CO 2 also mitigated the noxious effect of high O 3 on photosynthesis.

Although some molecular mechanisms underpinning CO 2 actions are unknown, the results presented highlight the importance of CO 2 as a regulator that mitigates the potential climate change-induced deleterious consequences in plants. Recent reports suggest that some CO 2 -associated responses may be mediated by NO.

Du et al. (2016) determined that 800 μmol.mol -1 of CO 2 increased the NO concentration in Arabidopsis leaves, through a mechanism related to nitrate availability. Moreover, NO increase, as a consequence of high CO 2 levels, was reported as a general procedure to improve iron (Fe) nutrition in response to Fe deficiency in tomato roots ( Jin et al., 2009 ).

The gas exchange between the atmosphere and plants is mainly regulated by stomata. But structure and physiology of stomata are also influenced by gasses ( García-Mata and Lamattina, 2013 ). Elevated CO 2 regulate stomatal density and conductance. Moreover, there is increasing evidence that this response is modified by interaction of CO 2 with other environmental factors ( Xu et al., 2016 ; Yan et al., 2017 ). Wang et al. (2015) reported that 800 μmol.mol -1 of CO 2 increases the NO concentration in A. thaliana guard cells, inducing stomatal closure. Both NR and NO synthase (NOS)-like activities are necessary for CO 2 -induced NO accumulation. Comprehensive pharmacological and genetic results obtained in Arabidopsis by Chater et al. (2015) , show that when CO 2 concentration is around 700–1000 ppm, stomatal density and closure are reduced. They also illustrate that those elements necessary for this process are: activation of both ABA biosynthesis genes and the PYR/RCAR ABA receptor, and ROS increase. However, Shi et al. (2015) provide genetic and pharmacological evidence that high CO 2 concentration induces stomatal closure by an ABA-independent mechanism in tomato. They show that 800 μmol.mol -1 of CO 2 increase the expression of the protein kinase OPEN STOMATA 1 (OST1), NOX, and nitrate reductase (NR) genes. They also show that the sequential production of NOX-dependent H 2 O 2 and NR-produced NO are mainly dependent of OST1, and are involved in the CO 2 -induced stomatal closure.

In ABA-dependent mechanisms, ABA is increased by CO 2. The binding of ABA to its receptor (PYR/RCAR) inactivates PP2C, activating OST1. In ABA-independent mechanism, OST1 will be transcriptionally induced by CO 2 . Once activated, OST1 along with Ca 2 + , activates NOX, increasing ROS ( Kim et al., 2010 ). The rise of guard cells ROS enhances NO, cytosolic free Ca 2 + , and pH ( Song et al., 2014 ; Xie et al., 2014 ). ROS and NO release Ca 2 + from internal reservoirs, or influx external Ca 2 + through plasma membrane Ca 2 + in channels. Cytosolic free Ca 2 + inactivate inward K + channels (K + in ) to prevent K + uptake and activate outward K + channels (K + out ) and Cl - (anion) channels (Cl - ) at the plasma membrane ( Blatt, 2000 ; García-Mata et al., 2003 ). Ca 2 + also activates slow anion channel homolog 3 (SLAH3), slow anion channel-associated 1 (SLAC1) and aluminum activated malate transporters (ALMT) ( Roelfsema et al., 2012 ). The consequence of the regulation of cation/anion channels is the net efflux of K + /Cl - /malate and influx of Ca 2 + , making guard cells lose turgor by water outlet, causing stomatal closure.

All together, the results discussed here suggest that CO 2 -induced NO increase is a common plant physiological response to oxidative stresses. Figure 2 shows the importance of CO 2 and NO in these processes.

FIGURE 2. Interplay between CO 2 and NO in plant redox physiology: CO 2 enters to the leaves by stomata. Once in mesophyll cells, CO 2 increase photosynthesis (PS) through the CO 2 -unsaturated Rubisco activity. When plants are in stress environments, ROS could be augmented by Rubisco-induced photorespiration and NADPH oxidase (NOX) activities. NOX- induced O 2 •– , in the apoplast is immediately transformed to H 2 O 2 by the superoxide dismutase (SOD). Plasma membrane is permeable to H 2 O 2 . CO 2 moderates oxidative stress in mesophyll cells by inhibiting both Rubisco photorespiration (PR) and NOX activities. Besides, NO is induced by CO 2 and ROS, alleviating the consequences of oxidative stress by scavenging ROS and activating or inhibiting the antioxidant system (AS). In guard cells, CO 2 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 Ca 2 + regulated ion channels induces stomatal closure, modulating O 3 and CO 2 uptake, decreasing evapotranspiration, and rising leaf temperature.

Abiotic Stress, ROS Generation, and Redox Balance: The Key Role of NO

Reactive oxygen species are generated in apoplast, plasma membrane, chloroplasts, mitochondria, and peroxisomes ( Farnese et al., 2016 ). It was proposed that each stress produces its own “ROS signature” ( Choudhury et al., 2017 ). For instance, drought may reduce the activity of Rubisco, decreasing CO 2 fixation and NADP+ regeneration by the Calvin cycle. As a consequence, chloroplast electron transport is altered, generating ROS by electron leakage to O 2 ( Carvalho, 2008 ). In drought stress, ROS increase is produced by NOX activity ( Farnese et al., 2016 ). In flooding, ROS generation is an ethylene-promoted process that involves calcium (Ca 2+ ) flux, and NOX activity ( Voesenek and Bailey-Serres, 2015 ).

In heat stress, a NOX-dependent transient ROS rise is an early event ( Königshofer et al., 2008 ). Then, endogenous ROS are sensed through histidine kinases, and an Arabidopsis heat stress factor (HsfA4a) appears to sense exogenous ROS. As a result, the MAPK signal pathway is activated ( Qu et al., 2013 ). Moreover, functional decrease in photosynthetic light reaction induces ROS concentration by high electron leakage from the thylakoid membrane ( Hasanuzzaman et al., 2013 ). In this process, O 2 is the acceptor, generating O 2 •– .

Thus, individual stresses or their different combinations may produce particular “ROS signatures.” Besides their deleterious effects, ROS are recognized as a signal in the plant reaction to biotic and abiotic stressors. ROS may induce programed cell death (PCD) to avoid pathogen spread ( Mur et al., 2008 ), trigger a systemic defense response signal ( Dubiella et al., 2013 ), or avoid the chloroplast antenna overloading by electrons divert ( Choudhury et al., 2017 ).

Whatever the origin and function, ROS concentration must be adequately regulated to avoid excessive concentration and consequent cellular damages. Depending on NO and ROS concentrations, NO has the dual capacity to activate or inhibit the ROS production, and is a key molecule for keeping cellular redox homeostasis under control ( Beligni and Lamattina, 1999a ; Correa-Aragunde et al., 2015 ). NO has a direct ROS-scavenging activity because it holds an unpaired electron, reaching elevated reactivity with O 2 , O 2 •– , and redox active metals. NO can mitigate OH formation by scavenging either Fe or O 2 •– ( Lamattina et al., 2003 ). However, NO reacting with ROS (mainly O 2 •– ) may generate reactive nitrogen species (RNS). An excess of RNS originates a nitrosative stress ( Corpas et al., 2011 ). To avoid the toxicity of nitrosative stress, NO is stored as GSNO in the cell.

GSH as a Redox Buffer. GSNO as NO Reservoir. SNO and S-Nitrosylation

Glutathione (GSH) is a small peptide with the sequence γ-l-glutamyl-l-cysteinyl-glycine that has a cell redox homeostatic impact in most plant tissues. It is a soluble small thiol considered a non-enzymatic antioxidant. It exists in the reduced (GSH) or oxidized state (GSSG), in which two GSH molecules are joined by a disulfide bond ( Rouhier et al., 2008 ). GSH alleviates oxidative damages in plants generated by abiotic stresses, including salinity, drought, higher, low temperature, and heavy metals. GSH is precursor of phytochelatins, polymers that chelate toxic metals and transport them to the vacuole ( Grill et al., 1989 ). Studies shown that GSH contributes to tolerate nickel, cadmium, zinc, mercury, aluminum and arsenate heavy metals in plants ( Asgher et al., 2017 ). Moreover, GSH has a role in the detoxification of ROS both directly, interacting with them, or indirectly, participating of enzymatic pathways. GSH is involved in glutathionylation, a posttranslational modification that causes a mixed disulfide bond between a Cys residue and GSH.

GSH can be oxidized to GSSG by H 2 O 2 and can react with NO to form the nitrosoglutathione (GSNO) derivative. GSNO is an intracellular NO reservoir. It is also a vehicle of NO throughout the cell and organs, spreading NO biological function. GSNO is the largest low-molecular-mass S-nitrosothiol (SNO) in plant cells ( Corpas et al., 2013 ). GSNO metabolism and its reaction with other molecules involve S-nitrosylation and S-transnitrosation which consist of the binding of a NO molecule to a cysteine residue in proteins. Thioredoxin produces protein denitrosylation ( Correa-Aragunde et al., 2013 ). GSNO could be decomposed by the GSNO reductase (GSNOR) to GSSG which, in turn, is reduced to GSH by glutathione reductase (GR).

Glutathione also participates in the GSH/ASC cycle, a series of enzymatic reactions that degrade H 2 O 2 . APX degrades H 2 O 2 using ASC, the other major antioxidant in plants, as cofactor. The oxidized ASC is reduced by monodehydroascorbate reductase (MDHAR) in an NAD(P)H-dependent manner and by dehydroascorbate reductase (DHAR) employing GSH as electron donor. The resulting GSSG is reduced in turn to GSH by GR ( Foyer and Noctor, 2011 ).

Different Effects of NO in the Regulation of Antioxidant Enzymes

The application of NO donors alleviates oxidative stress in plants challenged to abiotic and/or biotic stresses ( Laxalt et al., 1997 ; Beligni and Lamattina, 1999b , 2002 ; Shi et al., 2007 ; Xue et al., 2007 ; Leitner et al., 2009 ).

Besides the direct ROS-scavenging activity of NO, its beneficial effect is exerted by the regulation of the antioxidant enzymes activity that controls toxic levels of ROS and RNS ( Uchida et al., 2002 ; Shi et al., 2005 ; Song et al., 2006 ; Romero-Puertas et al., 2007 ; Bai et al., 2011 ). NO can modulate cell redox balance in plants through the regulation of gene expression, posttranslational modification or by its binding to the heme prosthetic group of some antioxidant enzymes.

SOD catalyzes the dismutation of stress-generated O 2 •– in one of two less harmful species: either molecular oxygen (O 2 ) or hydrogen peroxide (H 2 O 2 ). APX and CAT are the most important enzymes degrading H 2 O 2 in plants. They transform H 2 O 2 to H 2 O and O 2 . APX isoforms are primarily found in the cytosol and chloroplasts, while the CAT isoforms are found in peroxisomes. APX has strong affinity for H 2 O 2 and uses ASC as an electron donor. In contrast, CAT removes H 2 O 2 generated in the peroxisomal respiratory pathway without the need to reduce power. Even though CAT affinity for H 2 O 2 is low, its elevated rate of reaction offers an effective way to detoxify H 2 O 2 inside the cell. PRX may reduce both hydroperoxide and peroxynitrite.

Many reports on different plant species demonstrate that NO induces the transcription and activity of antioxidative enzymes in response to oxidative stress. The tolerance to drought and salt-induced oxidative stress in tobacco is related to the ABA-triggered production of H 2 O 2 and NO. In turn, they induce transcripts and activities of SOD, CAT, APX, and GR ( Zhang et al., 2009 ). UV-B-produced oxidative stress in Glycine max was alleviated by NO donors, which induced transcription and activities of SOD, CAT, and APX ( Santa-Cruz et al., 2014 ). Furthermore, in bean leaves, SOD, CAT, and APX activities are increased by NO donors, and protected from the oxidative stress generated by UV-B irradiation ( Shi et al., 2005 ). Drought tolerance in bermudagrass is improved by ABA-dependent SOD and CAT activities. This effect is regulated by H 2 O 2 and NO, NO acting downstream H 2 O 2 ( Lu et al., 2009 ).

Several antioxidant enzymes have been identified as target of S-nitrosylation, resulting in a change of their biological activity ( Romero-Puertas et al., 2008 ; Bai et al., 2011 ; Fares et al., 2011 ). For instance, NO reinforces recalcitrant seed desiccation tolerance in Antiaris toxicaria by activating the ascorbate-glutathione cycle through S-nitrosylation to control H 2 O 2 accumulation. Desiccation treatment reduced the level of S-nitrosylated APX, GR, and DHAR proteins. Instead, NO gas exposure activated them by S-nitrosylation ( Bai et al., 2011 ). Furthermore, APX was S-nitrosylated at Cys32 during saline stress and biotic stress, enhancing its enzymatic activity ( Begara-Morales et al., 2014 ; Yang et al., 2015 ). In addition, auxin-induced denitrosylation of cytosolic APX provoked inhibition of its activity, followed by an increase of H 2 O 2 concentration and the consequent lateral root formation in Arabidopsis ( Correa-Aragunde et al., 2013 ). Moreover, an inhibitory impact of S-nitrosylation on APX activity was also reported during programmed cell death in Arabidopsis ( de Pinto et al., 2013 ). CAT was identified to be S-nitrosylated in a proteomic study of isolated peroxisomes ( Ortega-Galisteo et al., 2012 ). A decrease of S-nitrosylated CAT under Cd treatment was reported. In addition, in vitro experiments demonstrated a reversible inhibitory effect of APX and CAT activities by NO binding to the Fe of the heme cofactor ( Brown, 1995 ; Clark et al., 2000 ). In addition, NOXs have been involved in plant defense, development, hormone biosynthesis and signaling ( Marino et al., 2012 ). Whereas S-nitrosylation did not affect SOD activities, nitration inhibited Mn-SOD1, Fe-SOD3, and CuZn-SOD3 activity to different degrees ( Holzmeister et al., 2015 ). SOD isoforms could also regulate endogenous NO availability by competing for the common substrate, O 2 •– , and it was demonstrated that bovine SOD may release NO from GSNO ( Singh et al., 1999 ). When GSNO is decomposed by GSNOR, it produces GSSG. GSNOR is also regulated by NO. Frungillo et al. (2014) demonstrated that NO-derived from nitrate assimilation in Arabidopsis inhibited GSNOR1 by S-nitrosylation, preventing GSNO degradation. They proposed that (S)NO controls its own generation and scavenging by modulating nitrate assimilation and GSNOR1 activity. It was also shown that chilling treatment in poplar increased S-nitrosylation of NR, along with a significant decrease of its activity ( Cheng et al., 2015 ).

The dual activity of Prx, suggests a role for this enzyme both in ROS and RNS regulation. S-nitrosylation of Arabidopsis PrxIIE inhibits its peroxynitrite activity, increasing peroxynitrite-mediated tyrosine nitration ( Romero-Puertas et al., 2007 ). Pea mitochondrial PrxIIF was S-nitrosylated under salt stress, and its peroxidase activity was reduced by 5 mM GSNO ( Camejo et al., 2013 ).

An interesting study demonstrated that NO controls hypersensitive response (HR) through S-nitrosylation of NOX, inhibiting ROS synthesis. This triggers a feedback loop limiting HR ( Yun et al., 2011 ).

Other proteins related to abiotic stress response are regulated by S-nitrosylation (For a review see Fancy et al., 2017 ).

Figure 3 is a simplified diagram that illustrates the main oxidative and nitrosative effects that modulate the activities of key cell components, thus maintaining cell redox balance. Note the feedback and positive-negative regulatory processes occurring in the main pathways. They involve posttranslational modifications that activate and inhibit the components involved in cell antioxidant system.

FIGURE 3. Molecules and mechanisms involved in NO-mediated redox balance. H 2 O 2 is generated mainly by NOX and SOD as a response to (a)biotic stress. APX and CAT are the main H 2 O 2 -degrading enzymes. NO is increased by H 2 O 2 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 H 2 O 2 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 O 2 •– reaction. SOD regulate RNS dismutating O 2 •– . Peroxiredoxins (Prx) reduce both ROS AND RNS. RNS are degraded by PrxIIe, and H 2 O 2 by PrxIIF. Both enzymes are inhibited by S-nitrosylation. Red lines: H 2 O 2 -regulated reactions. Purple lines: NO-regulated reactions. Green lines: GSNO-regulated reactions.

Conclusions and Perspectives

The accelerating rate of climate change, together with habitat fragmentation caused by human activity, are part of the selective pressures building a new Earth’s landscape.

Climate change is a multidimensional and simultaneous variation in duration, frequency and intensity of parameters like temperature and precipitation, altering the seasons and life on the Earth. In this scenario, plant species with increased adaptive plasticity will be better equipped to tolerate changes in the frequency of extreme weather events. GHG are one of the forces driving climate change. However, CO 2 and NO may contribute to maintaining the cell redox homeostasis, regulating the amount of ROS, GSH, GSNO, and SNO.

In this manuscript, we summarize the available evidence supporting the presence of broad spectrum anti-stress molecules, as NO in plants, for coping with unprecedented changes in environmental conditions. Future research should focus in better understanding the influence of GHG on plant physiology.

Author Contributions

RC conceived the project and wrote the manuscript. MN drew figures and collaborated in writing the manuscript. NC-A and LL supervised and complemented the drafting. All the persons entitled to authorship have been named and have approved the final version of the submitted manuscript.

This work was supported by grants from the Consejo Nacional de Investigaciones Cientificas y Tecnicas, the Agencia Nacional de Promoción Científica y Tecnológica, and the Universidad Nacional de Mar del Plata, Argentina. NC-A, LL, and RC are permanent members of the Scientific Research career of CONICET. MN is doctoral fellow of the ANPCYT.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The reviewer MCR-P and handling Editor declared their shared affiliation.

Acknowledgments

We thank ANPCYT for MN fellowship. We also thank Marta Terrazo for helping with the language revision of the manuscript.

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Keywords : climate change, greenhouse effect, oxidative stress, nitric oxide, plants

Citation: Cassia R, Nocioni M, Correa-Aragunde N and Lamattina L (2018) Climate Change and the Impact of Greenhouse Gasses: CO 2 and NO, Friends and Foes of Plant Oxidative Stress. Front. Plant Sci. 9:273. doi: 10.3389/fpls.2018.00273

Received: 18 November 2017; Accepted: 16 February 2018; Published: 01 March 2018.

Reviewed by:

Copyright © 2018 Cassia, Nocioni, Correa-Aragunde and Lamattina. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Raúl Cassia, [email protected]

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November 3, 2023

Earth Reacts to Greenhouse Gases More Strongly Than We Thought

Climate scientists, including pioneer James Hansen, are pinning down a fundamental factor that drives how hot Earth will get

By Chelsea Harvey & E&E News

A 'Blue Marble' image of the Earth taken from the VIIRS instrument aboard NASA's Earth-observing satellite – Suomi NPP.

NASA/NOAA/GSFC/Suomi NPP/VIIRS/Norman Kuring

CLIMATEWIRE |  Climate scientist James Hansen is frustrated. And he’s worried.

For nearly 40 years, Hansen has been warning the world of the dangers of global warming. His testimony at a groundbreaking 1988 Senate hearing on the greenhouse effect helped inject the coming climate crisis into the public consciousness. And it helped make him one of the most influential climate scientists in the world.

Hansen has spent several decades as director of NASA’s Goddard Institute for Space Studies, and now at 82, he directs Columbia University’s  Climate Science, Awareness and Solutions program .

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In the years since his seminal testimony, many of Hansen’s basic scientific predictions about the Earth’s climate future have come true. Greenhouse gas emissions have grown, and global temperatures have continued to rise. The world’s glaciers and ice sheets are melting and sea level rise is accelerating.

But Hansen has been disappointed with the scientific community’s response to some of his more recent projections about the future of the warming Earth, which some researchers have characterized as unrealistically dire.

In particular, he was discouraged by the response to a paper he published in 2016, suggesting catastrophic ice melt in Greenland and Antarctica, with widespread global effects, may be possible with relatively modest future warming.

Many researchers said such outcomes were unlikely. But Hansen described the paper as some of his most important work and a warning about the need for more urgent action.

Now he’s bracing himself for a similar reaction to his  latest paper , published Thursday morning.

“I expect the response to be characterized by scientific reticence,” he said in an email to E&E News.

The new paper, published in the research journal  Oxford Open Climate Change , addresses a central question in modern climate science: How much will the Earth warm in response to future carbon emissions? It’s a metric known as “climate sensitivity,” or how sensitive the planet is to greenhouse gases in the atmosphere.

Hansen’s findings suggest the planet may warm faster than previous estimates have indicated. And while some experts say it’s possible, others suggest that he’s taken the results too far.

In studies, scientists often tackle the climate sensitivity question by investigating how much the Earth would warm if atmospheric carbon dioxide concentrations doubled their preindustrial levels. Prior to the industrial era, global CO2 levels hovered around 280 parts per million, meaning a doubling would land around 560 ppm.

Today’s CO2 levels have already climbed above 400 ppm, giving the question a growing relevance.

Climate sensitivity is a difficult metric to estimate. It hinges on a wide variety of feedback loops in the Earth’s climate system, which can speed up or slow down the planet’s warming.

As the Earth’s reflective glaciers and ice sheets melt, for instance, the planet can absorb more sunlight and warm at a faster rate. Forests and other natural ecosystems may absorb different amounts of carbon as the planet warms. Different types of clouds can both speed up or slow down global warming, and it’s still unclear how they will change as the Earth heats up.

The uncertainties around these factors have made it challenging for scientists to pin down an exact estimate for climate sensitivity. But they’ve chipped away at it in recent years.

For decades, studies generally suggested that the Earth should experience anywhere from 1.5 to 4.5 degrees Celsius of warming with a doubling of CO2. But a  2020 paper narrowed the range  to between 2.6 and 3.9 C, using multiple lines of evidence including climate models, the Earth’s response to recent historical emissions and the Earth’s ancient climate history.

The latest assessment report from the U.N.’s Intergovernmental Panel on Climate Change adopted a similar estimate, suggesting a likely range of 2.5 to 4 C with a central estimate around 3 C.

Hansen’s new paper, published with an international group of co-authors, significantly ups the numbers. It suggests a central estimate of around 4.8 C, nearly 2 degrees higher than the IPCC’s figure.

The paper relies largely on evidence from Earth’s ancient climate history. One reason? It’s unclear whether current climate models accurately represent all the relevant feedback effects that may affect climate sensitivity, Hansen and his co-authors argue. The planet’s past provides a clearer view of how the Earth has responded to previous shifts in atmospheric carbon dioxide concentrations.

The paper also suggests that global warming is likely to proceed faster in the near term than previous studies have suggested.

Under the international Paris climate agreement, world leaders are striving to keep global warming well below 2 C and below 1.5 C if at all possible. The new paper warns that warming could exceed 1.5 C by the end of the 2020s and 2 C by 2050.

A gradual global decline in air pollution, driven by tightening environmental regulations, is part of the reasoning. Some types of air pollution are known to have a cooling effect on the climate, which may mask some of the impact of greenhouse gas emissions. As these aerosols decline in the atmosphere, some research suggests, this masking effect may fall away and global temperatures may rise at faster rates.

Hansen and his co-authors argue that better accounting for the declines in global aerosols should accelerate estimates of near-term global warming. Studies suggest that warming between 1970 and 2010 likely proceeded at around 0.18 C per decade. Post-2010, the new paper argues, that figure should rise to 0.27 C.

The findings should motivate greater urgency to not only cut greenhouse gas emissions but to eventually lower global temperatures closer to their preindustrial levels, Hansen suggests. That means using natural resources and technological means to remove carbon dioxide from the atmosphere.

Hansen also suggests that a controversial form of geoengineering, known as solar radiation management, is likely warranted. SRM, in theory, would use reflective aerosols to beam sunlight away from the Earth and lower the planet’s temperatures. The practice has not been tested at any large scale, and scientists have raised a variety of concerns about its ethics and potential unintended side effects.

Yet Hansen believes scientists and activists “should raise concerns about the safety and ethics of NOT doing SRM,” he said by email.

Climate change, caused by human greenhouse gas emissions, is in itself a form of planetary geoengineering, he added.

“My suggestion is to reduce human geoengineering of the planet,” he said.

Yet some scientists say the new paper’s findings — again — are overblown.

The paper “adds very little to the literature,” said Piers Forster, director of the Priestly International Centre for Climate at Leeds University in the U.K. and a lead chapter author of the IPCC’s latest assessment report, in an email to E&E News.

It presents high-end estimates of climate sensitivity based on ancient climate records from the Earth’s past — but those findings aren’t necessarily new, he said. Forster also suggested that some of the methods the new paper used to arrive at those high estimates were “quite subjective and not justified by observations, model studies or literature.”

Forster also took issue with the new paper’s treatment of previous climate sensitivity estimates, including the widely cited 2020 study, which the authors suggested were far too low. The 2020 study presented a careful analysis, using multiple lines of high-quality evidence, Forster said. And yet the authors of the new paper “dismiss it, on spurious grounds.”

Michael Oppenheimer, a climate scientist and director of the Center for Policy Research on Energy and Environment at Princeton University, said the uncertainties around the effects of declining aerosols were important to pay attention to. And he suggested that the new paper’s climate sensitivity estimates were possible.

But added that he regards them as “a worst-worst-case” scenario.

“I think it’s perfectly legitimate to have a worst-worst-case out there,” he added. “They help people think about what the boundaries of the possible are, and they are necessary for risk management against the climate problem.”

But there are still so many uncertainties about the kinds of feedback factors affecting the Earth’s climate sensitivity, he said, that “you can’t really nail it down with the kind of precision that [Hansen’s] provided.”

But Hansen says the new paper’s lines of evidence are based on the most up-to-date research on the Earth’s ancient history.

“[T]here is no basis whatever for the claim that our results are ‘unlikely,’” he said by email. “It is the IPCC sensitivity that is unlikely, less than 1 percent chance of being right, as we show quantitatively in our (peer-reviewed) paper.”

Hansen and 'scientific reticence'

Hansen has been into the deep end of climate debates for much of his career.

In 1988, at the time of his Senate testimony, scientists were still discussing whether the fingerprint of human-caused global warming could yet be detected above the “noise” of the Earth’s natural climate variations.

“When I first got into this, and when Jim and I were testifying, we were arguing about whether there's a global signal,” said Oppenheimer, the Princeton scientist, who testified alongside Hansen in 1988. “All the information we had was about global mean temperature, global mean sea level. We couldn’t talk in the language of things that people cared about.”

But even with the limitations of climate science at the time, the scientists warned the world of the dangers to come.

Hansen has co-authored dozens of papers on climate change in the years since, many of which have been highly regarded by the scientific community.

“Over time, he’s got a pretty damn good track record of turning out to be right about things that other people thought differently about,” Oppenheimer said.

Forster, the Leeds University scientist, agreed that “some of Hansen’s papers are brilliant and his work and deeds helped establish this IPCC in the first place.”

But he added that he still thought the new paper misses the mark.

The reception is similar to a major paper Hansen published in 2016, widely known as the  “Ice Melt” paper.

The Ice Melt paper, published in the journal  Atmospheric Chemistry and Physics , provided a grim, sweeping vision of the Earth’s climate future, focused on the consequences of the melting Greenland and Antarctic ice sheets. Drawing largely on ancient climate data — similar to the new paper — it warned of rapid melting and sea-level rise on the order of several meters within the next century.

It also suggested that the rapid influx of cold, fresh meltwater into the sea could affect ocean circulation patterns and even cause a giant Atlantic current to shut down. That’s a controversial prediction  deemed unlikely by the IPCC , one that would have severe impacts on global weather and climate patterns if it actually happened.

The paper received mixed reactions from other climate scientists upon publication. Some praised the paper, while many suggested the findings were unrealistic.

Another 2016 paper , published by a different group of scientists, later found that the likelihood of an Atlantic current shutdown was relatively small and suggested that Hansen’s paper relied on “unrealistic assumptions.”

In his new paper, Hansen referred to that study as an “indictment” of Ice Melt. He also noted that the IPCC’s latest assessment report did not include Ice Melt’s predictions, an omission he likened in the new paper to a form of censorship.

“Science usually acknowledges alternative views and grants ultimate authority to nature,” the new paper states. “In the opinion of our first author (Hansen), IPCC does not want its authority challenged and is comfortable with gradualism. Caution has merits, but the delayed response and amplifying feedbacks of climate make excessive reticence a danger.”

Responding to critiques of his new paper, Hansen again suggested that “scientific reticence” — or a kind of resistance to new findings — is at play. He pointed to a  1961 paper by sociologist Bernard Barber  suggesting that scientists themselves can be resistant to scientific discovery.

Claims that his new findings are unrealistic, Hansen said, are “a perfect example of the category of scientific reticence that Barber describes as ‘resistance to discovery.’ It takes a long time for new results to sink into the community.”

Resistance to scientific findings is nothing new to Hansen. His 1988 testimony initially shook the political establishment — yet decades later, global climate action is still proceeding too slowly to meet the Paris climate targets.

When he first testified to Congress in the 1980s, Oppenheimer said, he expected that world governments would have started meaningful emissions reduction programs by the year 2000 or so.

“We didn’t get ahead of the impacts,” he said. “And that’s probably because people weren't willing to support strong governmental action in most countries … until they were getting clobbered by unusual and highly damaging, and in some cases unprecedented, climate events.”

He regards the current state of global climate action now with a mix of skepticism and optimism.

“We’re in the process of muddling through — we’re in a period where climate change is gonna be painful for a while, it’s gonna hurt a lot of people in a lot of places, but we can get out the other side,” he said. “I think we can get there. But will we?”

Hansen echoed his sentiments in starker terms.

He wrote that he’s been surprised by “the increase of anti-science no-nothing thinking in our politics.”

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• Published: 14 December 1989

Observational determination of the greenhouse effect

• A. Raval 1 &
• V. Ramanathan 1  

Nature volume  342 ,  pages 758–761 ( 1989 ) Cite this article

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Satellite measurements are used to quantify the atmospheric greenhouse effect, defined here as the infrared radiation energy trapped by atmospheric gases and clouds. The greenhouse effect is found to increase significantly with sea surface temperature. The rate of increase gives compelling evidence for the positive feedback between surface temperature, water vapour and the green-house effect; the magnitude of the feedback is consistent with that predicted by climate models. This study demonstrates an effective method for directly monitoring, from space, future changes in the greenhouse effect.

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Global warming at near-constant tropospheric relative humidity is supported by observations

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Raval, A., Ramanathan, V. Observational determination of the greenhouse effect. Nature 342 , 758–761 (1989). https://doi.org/10.1038/342758a0

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Climate Change: Evidence and Causes: Update 2020 (2020)

Chapter: conclusion, c onclusion.

This document explains that there are well-understood physical mechanisms by which changes in the amounts of greenhouse gases cause climate changes. It discusses the evidence that the concentrations of these gases in the atmosphere have increased and are still increasing rapidly, that climate change is occurring, and that most of the recent change is almost certainly due to emissions of greenhouse gases caused by human activities. Further climate change is inevitable; if emissions of greenhouse gases continue unabated, future changes will substantially exceed those that have occurred so far. There remains a range of estimates of the magnitude and regional expression of future change, but increases in the extremes of climate that can adversely affect natural ecosystems and human activities and infrastructure are expected.

Citizens and governments can choose among several options (or a mixture of those options) in response to this information: they can change their pattern of energy production and usage in order to limit emissions of greenhouse gases and hence the magnitude of climate changes; they can wait for changes to occur and accept the losses, damage, and suffering that arise; they can adapt to actual and expected changes as much as possible; or they can seek as yet unproven “geoengineering” solutions to counteract some of the climate changes that would otherwise occur. Each of these options has risks, attractions and costs, and what is actually done may be a mixture of these different options. Different nations and communities will vary in their vulnerability and their capacity to adapt. There is an important debate to be had about choices among these options, to decide what is best for each group or nation, and most importantly for the global population as a whole. The options have to be discussed at a global scale because in many cases those communities that are most vulnerable control few of the emissions, either past or future. Our description of the science of climate change, with both its facts and its uncertainties, is offered as a basis to inform that policy debate.

A CKNOWLEDGEMENTS

The following individuals served as the primary writing team for the 2014 and 2020 editions of this document:

• Eric Wolff FRS, (UK lead), University of Cambridge
• Inez Fung (NAS, US lead), University of California, Berkeley
• Brian Hoskins FRS, Grantham Institute for Climate Change
• John F.B. Mitchell FRS, UK Met Office
• Tim Palmer FRS, University of Oxford
• Benjamin Santer (NAS), Lawrence Livermore National Laboratory
• John Shepherd FRS, University of Southampton
• Keith Shine FRS, University of Reading.
• Susan Solomon (NAS), Massachusetts Institute of Technology
• Kevin Trenberth, National Center for Atmospheric Research
• John Walsh, University of Alaska, Fairbanks
• Don Wuebbles, University of Illinois

Staff support for the 2020 revision was provided by Richard Walker, Amanda Purcell, Nancy Huddleston, and Michael Hudson. We offer special thanks to Rebecca Lindsey and NOAA Climate.gov for providing data and figure updates.

The following individuals served as reviewers of the 2014 document in accordance with procedures approved by the Royal Society and the National Academy of Sciences:

• Richard Alley (NAS), Department of Geosciences, Pennsylvania State University
• Alec Broers FRS, Former President of the Royal Academy of Engineering
• Harry Elderfield FRS, Department of Earth Sciences, University of Cambridge
• Joanna Haigh FRS, Professor of Atmospheric Physics, Imperial College London
• Isaac Held (NAS), NOAA Geophysical Fluid Dynamics Laboratory
• John Kutzbach (NAS), Center for Climatic Research, University of Wisconsin
• Jerry Meehl, Senior Scientist, National Center for Atmospheric Research
• John Pendry FRS, Imperial College London
• John Pyle FRS, Department of Chemistry, University of Cambridge
• Gavin Schmidt, NASA Goddard Space Flight Center
• Emily Shuckburgh, British Antarctic Survey
• Gabrielle Walker, Journalist
• Andrew Watson FRS, University of East Anglia

The Support for the 2014 Edition was provided by NAS Endowment Funds. We offer sincere thanks to the Ralph J. and Carol M. Cicerone Endowment for NAS Missions for supporting the production of this 2020 Edition.

F OR FURTHER READING

For more detailed discussion of the topics addressed in this document (including references to the underlying original research), see:

• Intergovernmental Panel on Climate Change (IPCC), 2019: Special Report on the Ocean and Cryosphere in a Changing Climate [ https://www.ipcc.ch/srocc ]
• National Academies of Sciences, Engineering, and Medicine (NASEM), 2019: Negative Emissions Technologies and Reliable Sequestration: A Research Agenda [ https://www.nap.edu/catalog/25259 ]
• Royal Society, 2018: Greenhouse gas removal [ https://raeng.org.uk/greenhousegasremoval ]
• U.S. Global Change Research Program (USGCRP), 2018: Fourth National Climate Assessment Volume II: Impacts, Risks, and Adaptation in the United States [ https://nca2018.globalchange.gov ]
• IPCC, 2018: Global Warming of 1.5°C [ https://www.ipcc.ch/sr15 ]
• USGCRP, 2017: Fourth National Climate Assessment Volume I: Climate Science Special Reports [ https://science2017.globalchange.gov ]
• NASEM, 2016: Attribution of Extreme Weather Events in the Context of Climate Change [ https://www.nap.edu/catalog/21852 ]
• IPCC, 2013: Fifth Assessment Report (AR5) Working Group 1. Climate Change 2013: The Physical Science Basis [ https://www.ipcc.ch/report/ar5/wg1 ]
• NRC, 2013: Abrupt Impacts of Climate Change: Anticipating Surprises [ https://www.nap.edu/catalog/18373 ]
• NRC, 2011: Climate Stabilization Targets: Emissions, Concentrations, and Impacts Over Decades to Millennia [ https://www.nap.edu/catalog/12877 ]
• Royal Society 2010: Climate Change: A Summary of the Science [ https://royalsociety.org/topics-policy/publications/2010/climate-change-summary-science ]
• NRC, 2010: America’s Climate Choices: Advancing the Science of Climate Change [ https://www.nap.edu/catalog/12782 ]

Much of the original data underlying the scientific findings discussed here are available at:

• https://data.ucar.edu/
• https://climatedataguide.ucar.edu
• https://iridl.ldeo.columbia.edu
• https://ess-dive.lbl.gov/
• https://www.ncdc.noaa.gov/
• https://www.esrl.noaa.gov/gmd/ccgg/trends/
• http://scrippsco2.ucsd.edu
• http://hahana.soest.hawaii.edu/hot/

Climate change is one of the defining issues of our time. It is now more certain than ever, based on many lines of evidence, that humans are changing Earth's climate. The Royal Society and the US National Academy of Sciences, with their similar missions to promote the use of science to benefit society and to inform critical policy debates, produced the original Climate Change: Evidence and Causes in 2014. It was written and reviewed by a UK-US team of leading climate scientists. This new edition, prepared by the same author team, has been updated with the most recent climate data and scientific analyses, all of which reinforce our understanding of human-caused climate change.

Scientific information is a vital component for society to make informed decisions about how to reduce the magnitude of climate change and how to adapt to its impacts. This booklet serves as a key reference document for decision makers, policy makers, educators, and others seeking authoritative answers about the current state of climate-change science.

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Impact of plant community diversity on greenhouse gas emissions in riparian zones.

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Li, G.; Xu, J.; Tang, Y.; Wang, Y.; Lou, J.; Xu, S.; Iqbal, B.; Li, Y.; Du, D. Impact of Plant Community Diversity on Greenhouse Gas Emissions in Riparian Zones. Plants 2024 , 13 , 2412. https://doi.org/10.3390/plants13172412

Li G, Xu J, Tang Y, Wang Y, Lou J, Xu S, Iqbal B, Li Y, Du D. Impact of Plant Community Diversity on Greenhouse Gas Emissions in Riparian Zones. Plants . 2024; 13(17):2412. https://doi.org/10.3390/plants13172412

Li, Guanlin, Jiacong Xu, Yi Tang, Yanjiao Wang, Jiabao Lou, Sixuan Xu, Babar Iqbal, Yingnan Li, and Daolin Du. 2024. "Impact of Plant Community Diversity on Greenhouse Gas Emissions in Riparian Zones" Plants 13, no. 17: 2412. https://doi.org/10.3390/plants13172412

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The Greenhouse Effect and our Planet

The greenhouse effect happens when certain gases, which are known as greenhouse gases, accumulate in Earth’s atmosphere. Greenhouse gases include carbon dioxide (CO 2 ), methane (CH 4 ), nitrous oxide (N 2 O), ozone (O 3 ), and fluorinated gases.

Biology, Ecology, Earth Science, Geography, Human Geography

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The greenhouse effect happens when certain gases , which are known as greenhouse gases , accumulate in Earth’s atmosphere . Greenhouse gases include carbon dioxide (CO 2 ), methane (CH 4 ), nitrous oxide (N 2 O), ozone (O 3 ), and fluorinated gases.

Greenhouse gases allow the sun’s light to shine onto Earth’s surface, and then the gases, such as ozone, trap the heat that reflects back from the surface inside Earth’s atmosphere. The gases act like the glass walls of a greenhouse—thus the name, greenhouse gas

According to scientists, the average temperature of Earth would drop from 14˚C (57˚F) to as low as –18˚C (–0.4˚F), without the greenhouse effect.

Some greenhouse gases come from natural sources, for example, evaporation  adds water vapor to the atmosphere. Animals and plants release carbon dioxide when they respire, or breathe. Methane is released naturally from decomposition. There is evidence that suggests methane is released in low-oxygen environments , such as  swamps or landfills . Volcanoes —both on land and under the ocean —release greenhouse gases, so periods of high volcanic activity tend to be warmer.

Since the  Industrial Revolution  of the late 1700s and early 1800s, people have been releasing larger quantities of greenhouse gases into the atmosphere. That amount has skyrocketed in the past century. Greenhouse gas emissions increased 70 percent between 1970 and 2004. Emissions of CO 2 , rose by about 80 percent during that time.

The amount of CO 2 in the atmosphere far exceeds the naturally occurring range seen during the last 650,000 years.

Most of the CO 2 that people put into the atmosphere comes from burning  fossil fuels . Cars, trucks, t rains , and planes all burn fossil fuels. Many electric power plants do as well. Another way humans release CO 2 into the atmosphere is by cutting down  forests , because trees contain large amounts of carbon.

People add methane to the atmosphere through  livestock  farming, landfills, and fossil fuel production such as  coal mining  and natural gas processing. Nitrous oxide comes from  agriculture  and fossil fuel burning. Fluorinated gases include chlorofluorocarbons (CFCs),  hydrochlorofluorocarbons (HCFCs), and hydrofluorocarbons (HFCs). They are produced during the manufacturing of refrigeration and cooling products and through aerosols.

All of these human activities add greenhouse gases to the atmosphere. As the level of these gases rises, so does the temperature of Earth. The rise in Earth’s average temperature contributed to by human activity is known as  global warming .

The Greenhouse Effect and Climate Change Even slight increases in average global temperatures can have huge effects.

Perhaps the biggest, most obvious effect is that  glaciers and  ice caps melt faster than usual. The  meltwater  drains into the oceans, causing  sea levels to rise.

Glaciers and ice caps cover about 10 percent of the world’s landmasses. They hold between 70 and 75 percent of the world’s  freshwater . If all of this ice melted, sea levels would rise by about 70 meters (230 feet).

The Intergovernmental Panel on Climate Change states that the global sea level rose about 1.8 millimeters (0.07 inches) per year from 1961 to 1993, and about 3.1 millimeters (0.12 inches) per year since 1993.

Rising sea levels cause  flooding in  coastal cities, which could displace millions of people in low-lying areas such as Bangladesh, the U.S. state of Florida, and the Netherlands.

Millions more people in countries like Bolivia, Peru, and India depend on glacial meltwater for drinking,  irrigation , and  hydroelectric power . Rapid loss of these glaciers would devastate those countries.

Greenhouse gas emissions affect more than just temperature. Another effect involves changes in  precipitation , such as rain and  snow .

Over the course of the 20th century, precipitation increased in eastern parts of North and South America, northern Europe, and northern and central Asia. However, it has decreased in parts of Africa, the Mediterranean, and southern Asia.

As climates change, so do the habitats for living things. Animals that are adapted to a certain climate may become threatened. Many human societies depend on predictable rain patterns in order to grow specific  crops for food, clothing, and trade. If the climate of an area changes, the people who live there may no longer be able to grow the crops they depend on for survival. Some scientists also worry that tropical diseases will expand their ranges into what are now more temperate regions if the temperatures of those areas increase.

Most climate scientists agree that we must reduce the amount of greenhouse gases released into the atmosphere. Ways to do this, include:

• driving less, using public transportation , carpooling, walking, or riding a bike.
• flying less—airplanes produce huge amounts of greenhouse gas emissions.
• reducing, reusing, and recycling.
• planting a tree—trees absorb carbon dioxide, keeping it out of the atmosphere.
• using less  electricity .
• eating less meat—cows are one of the biggest methane producers.
• supporting alternative energy sources that don’t burn fossil fuels.

Artificial Gas

Chlorofluorocarbons (CFCs) are the only greenhouse gases not created by nature. They are created through refrigeration and aerosol cans.

CFCs, used mostly as refrigerants, are chemicals that were developed in the late 19th century and came into wide use in the mid-20th century.

Other greenhouse gases, such as carbon dioxide, are emitted by human activity, at an unnatural and unsustainable level, but the molecules do occur naturally in Earth's atmosphere.

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