NO and H2S Contribute to Crop Resilience against Atmospheric Stressors

Atmospheric stressors include a variety of pollutant gases such as CO2, nitrous oxide (NOx), and sulfurous compounds which could have a natural origin or be generated by uncontrolled human activity. Nevertheless, other atmospheric elements including high and low temperatures, ozone (O3), UV-B radiation, or acid rain among others can affect, at different levels, a large number of plant species, particularly those of agronomic interest. Paradoxically, both nitric oxide (NO) and hydrogen sulfide (H2S), until recently were considered toxic since they are part of the polluting gases; however, at present, these molecules are part of the mechanism of response to multiple stresses since they exert signaling functions which usually have an associated stimulation of the enzymatic and non-enzymatic antioxidant systems. At present, these gasotransmitters are considered essential components of the defense against a wide range of environmental stresses including atmospheric ones. This review aims to provide an updated vision of the endogenous metabolism of NO and H2S in plant cells and to deepen how the exogenous application of these compounds can contribute to crop resilience, particularly, against atmospheric stressors stimulating antioxidant systems.


Introduction
Higher plants, as sessile organisms, are recurrently subjected to environmental changes throughout their life cycle.Among the different atmospheric stressors, it can be mentioned that high and low temperatures, hailstorms, absence of rain (drought), extreme rain (waterlogging), ozone, ultraviolet (UV-B) radiation, CO 2 , methane, or nitrogen oxide (NOx) among others which effects on plants can be increased under the current climate change pattern [1][2][3].The majority of them have a natural origin, but the negative effects of some of them could be increased by human activity.Furthermore, these atmospheric pollutants can affect extensive areas, but others can affect more restricted areas due to local phenomena, for example, the emissions of polluting gases by volcanoes or certain industries.However, the degree of pollution effects on a specific plant will depend on its intensity and the distance from the emission source.
Nitric oxide ( • NO) is a free radical that is part of the nitrogen cycle and in the atmosphere, in the presence of oxygen, it quickly transforms into nitrogen dioxide ( • NO 2 ), and both constitute nitrogen oxide (NOx).Figure 1a,b illustrates how atmospheric • NO, as a pollutant, participates in the formation of acid rain as well as in the destruction of the ozone layer [4,5].For many plant species, the negative effects triggered by nitrogen oxides (NOx) have been estimated when the level of NOx is around 30 µg/m 3 .However, there is experimental evidence suggesting that moderate concentrations of NOx may have both positive and negative plant growth responses [6,7].
On the other hand, atmospheric hydrogen sulfide (H 2 S) comes from different sources such as volcanoes, geothermal vents, or wetlands where it is generated by bacteria during the anaerobic decay of organic sulfur compounds [8][9][10].In the atmosphere, H 2 S is oxidized to sulfur dioxide (SO 2 ), which then can be converted to sulfuric acid (H 2 SO 4 ) and participates in acid rain (Figure 1a).
Int. J. Mol.Sci.2024, 25, x FOR PEER REVIEW 2 of 14 On the other hand, atmospheric hydrogen sulfide (H2S) comes from different sources such as volcanoes, geothermal vents, or wetlands where it is generated by bacteria during the anaerobic decay of organic sulfur compounds [8][9][10].In the atmosphere, H2S is oxidized to sulfur dioxide (SO2), which then can be converted to sulfuric acid (H2SO4) and participates in acid rain (Figure 1a).N2) has a greater presence in the atmosphere but in the occurrence of atmospheric oxygen, it quickly transforms into nitrogen dioxide ( • NO2).Nitrogen oxides are acidic, and they can form nitric acid (HNO3) which can be dissolved in water, giving rise to acid rain.Similarly, H2S can also react with O2 to generate sulfur dioxide (SO2) which reacts with water droplets in clouds to create sulfuric acid (H2SO4).(b) • NO2 due to ultraviolet (UV) radiation generates • NO and atomic oxygen, which together with O2 generates ozone, which reacts with • NO, generating • NO2 and oxygen, which constitutes the photolytic cycle of the destruction of the O3 layer.
From the time when • NO and H2S were identified and characterized in the 18th century, these molecules have been considered toxic molecules that exert negative effects on all organisms.At the end of the 20th century, it was found that • NO and H2S can be generated endogenously in both animal and plant cells [11][12][13][14].As a result, the concept of "toxic" molecules changed, and to date, they have been shown to both exert regulatory and signaling functions in many plant processes such as seed germination, root development, plant growth, stomatal movement, senescence, fruit development and ripening as well as response mechanisms to both abiotic and biotic stresses [15][16][17].Thus, both • NO and H2S have paradoxical effects as atmospheric pollutants but also as signaling molecules that are endogenously generated in cells.Likewise, there are numerous examples that their exogenous application, individually or in combination, exerts beneficial effects against atmospheric stress.This review aims to provide an updated vision of the endogenous metabolism of • NO and H2S in plant cells and to deepen how the exogenous application of these compounds can contribute to crop resilience against some representative atmospheric stressors such as extreme temperature, O3, UV-B radiation, and acid rain.From the time when • NO and H 2 S were identified and characterized in the 18th century, these molecules have been considered toxic molecules that exert negative effects on all organisms.At the end of the 20th century, it was found that • NO and H 2 S can be generated endogenously in both animal and plant cells [11][12][13][14].As a result, the concept of "toxic" molecules changed, and to date, they have been shown to both exert regulatory and signaling functions in many plant processes such as seed germination, root development, plant growth, stomatal movement, senescence, fruit development and ripening as well as response mechanisms to both abiotic and biotic stresses [15][16][17].Thus, both • NO and H 2 S have paradoxical effects as atmospheric pollutants but also as signaling molecules that are endogenously generated in cells.Likewise, there are numerous examples that their exogenous application, individually or in combination, exerts beneficial effects against atmospheric stress.This review aims to provide an updated vision of the endogenous metabolism of • NO and H 2 S in plant cells and to deepen how the exogenous application of these compounds can contribute to crop resilience against some representative atmospheric stressors such as extreme temperature, O 3 , UV-B radiation, and acid rain.

• NO and H 2 S Metabolism in Higher Plants
Our knowledge about • NO and H 2 S metabolism has increased significantly during the last decade considering that these two molecules were considered toxic until they were found to be endogenously generated in animal cells [13,14].
The enzymatic generation of • NO in higher plants has been very controversial since its generation was discovered.Currently, two main enzymatic pathways have been generally accepted, the reductive and the oxidative pathways [18][19][20].The reductive pathway is the one that uses nitrate and nitrite as substrates using NADH as an electron donor, being linked to the nitrate reductase (NR) and nitrite reductase (NiR) activities [21][22][23][24].On the other hand, there is the oxidative pathway, which is considered similar to the nitric oxide synthase (NOS) of animal cells, since it starts with L-arginine using NADPH as the electron donor and FAD, FMN, calcium, calmodulin, and tetrabiopterin as cofactors, so it is called L-Arg-dependent NOS-like activity because the gene similar to that of animal organisms that encodes it has not been identified [25][26][27].In addition, there is another possible route that, from polyamines or oximes, seems to be involved in the generation of • NO [28][29][30].However, we must not rule out other possible enzymatic or non-enzymatic sources that should be involved in the generation of • NO.
The generation of H 2 S in plants is part of the sulfate assimilation pathway and the cysteine biosynthesis pathway.Currently, there are several enzymes located in different subcellular compartments involved in the generation of H 2 S [31,32].Figure 2a,b shows the main enzymatic source involved in the generation of • NO and H 2 S in higher plants.

• NO and H2S Metabolism in Higher Plants
Our knowledge about • NO and H2S metabolism has increased significantly during the last decade considering that these two molecules were considered toxic until they were found to be endogenously generated in animal cells [13,14].
The enzymatic generation of • NO in higher plants has been very controversial since its generation was discovered.Currently, two main enzymatic pathways have been generally accepted, the reductive and the oxidative pathways [18][19][20].The reductive pathway is the one that uses nitrate and nitrite as substrates using NADH as an electron donor, being linked to the nitrate reductase (NR) and nitrite reductase (NiR) activities [21][22][23][24].On the other hand, there is the oxidative pathway, which is considered similar to the nitric oxide synthase (NOS) of animal cells, since it starts with L-arginine using NADPH as the electron donor and FAD, FMN, calcium, calmodulin, and tetrabiopterin as cofactors, so it is called L-Arg-dependent NOS-like activity because the gene similar to that of animal organisms that encodes it has not been identified [25][26][27].In addition, there is another possible route that, from polyamines or oximes, seems to be involved in the generation of • NO [28][29][30].However, we must not rule out other possible enzymatic or non-enzymatic sources that should be involved in the generation of • NO.
The generation of H2S in plants is part of the sulfate assimilation pathway and the cysteine biosynthesis pathway.Currently, there are several enzymes located in different subcellular compartments involved in the generation of H2S [31,32].Figure 2a,b shows the main enzymatic source involved in the generation of • NO and H2S in higher plants.

• NO-and H2S-Derived Posttranslational Modifications (PTMs) as Tools to Regulate Plant Metabolism
• NO and derived molecules called reactive nitrogen species (RNS) can affect the function of different macromolecules through their specific interactions.Among the RNS, it is worth highlighting peroxynitrite (ONOO − ) which is the result of the chemical reac-

• NO-and H 2 S-Derived Posttranslational Modifications (PTMs) as Tools to Regulate Plant Metabolism
• NO and derived molecules called reactive nitrogen species (RNS) can affect the function of different macromolecules through their specific interactions.Among the RNS, it is worth highlighting peroxynitrite (ONOO − ) which is the result of the chemical reaction between • NO and superoxide radical (O 2 •− ) [33] or S-nitrosoglutathione (GSNO), which results from the interaction of • NO with reduced glutathione (GSH) [34,35].RNS can mediate several post-translational modifications (PTMs) that affect different macromolecules including peptides, proteins, fatty acids, and nucleotides.Thus, RNS interacts with thiol groups present in Cys residues to generate the corresponding S-nitrosated protein, with tyrosine residues to generate tyrosine nitration or bind to metals present in certain proteins in a process designed as metal nitrosylation [36][37][38][39].• NO can also interact with other biomolecules including unsaturated fatty acids (FAs) to form the corresponding nitro-FAs [40] and nucleic acids through guanine or guanosine to generate 8-nitroguanine or 8-nitroguanosine, respectively [41,42].
H 2 S mediates another PTM named persulfidation which involves its interaction with the thiol group (-SH) of susceptible Cys residues.Similar to S-nitrosation, persulfidation is a reversible covalent interaction but, in this case, the thiol group is converted into a persulfide (-SSH) group which can affect positively or negatively the function of the target proteins [43,44].Figure 3 illustrates the main PTMs mediated by • NO and H 2 S.However, in a cellular context, it should be considered that the thiol groups of Cys residues are susceptible to being targets of other thiol-based oxidative posttranslational modifications (OxiPTMs) mediated by glutathione (S-glutathionylation), H 2 O 2 (S-sulfenylation), fatty acids (S-acylation) or cyanide (S-cyanylation) that can compete with each other depending on their cellular concentrations and the subcellular location of the target protein [45][46][47][48][49].However, in conditions of oxidative stress resulting from environmental stress, some of them may have a greater preponderance, such as an increase in H 2 O 2 .
tion between • NO and superoxide radical (O2 •− ) [33] or S-nitrosoglutathione (GSNO), which results from the interaction of • NO with reduced glutathione (GSH) [34,35].RNS can mediate several post-translational modifications (PTMs) that affect different macromolecules including peptides, proteins, fatty acids, and nucleotides.Thus, RNS interacts with thiol groups present in Cys residues to generate the corresponding S-nitrosated protein, with tyrosine residues to generate tyrosine nitration or bind to metals present in certain proteins in a process designed as metal nitrosylation [36][37][38][39].• NO can also interact with other biomolecules including unsaturated fatty acids (FAs) to form the corresponding nitro-FAs [40] and nucleic acids through guanine or guanosine to generate 8-nitroguanine or 8-nitroguanosine, respectively [41,42].
H2S mediates another PTM named persulfidation which involves its interaction with the thiol group (-SH) of susceptible Cys residues.Similar to S-nitrosation, persulfidation is a reversible covalent interaction but, in this case, the thiol group is converted into a persulfide (-SSH) group which can affect positively or negatively the function of the target proteins [43,44].Figure 3 illustrates the main PTMs mediated by • NO and H2S.However, in a cellular context, it should be considered that the thiol groups of Cys residues are susceptible to being targets of other thiol-based oxidative posttranslational modifications (OxiPTMs) mediated by glutathione (S-glutathionylation), H2O2 (S-sulfenylation), fatty acids (S-acylation) or cyanide (S-cyanylation) that can compete with each other depending on their cellular concentrations and the subcellular location of the target protein [45][46][47][48][49].However, in conditions of oxidative stress resulting from environmental stress, some of them may have a greater preponderance, such as an increase in H2O2.

Stomata Movement, a Process Regulated by • NO and H2S
Stomata are specialized cells that regulate gas exchange in the leaves and stomatal closure is one of the response mechanisms against atmospheric stress [50][51][52].It is interesting to mention that both • NO and H2S are molecules that, although they may be polluting molecules, are also generated endogenously by regulating stomatal closure through PTMs including tyrosine nitration, S-nitrosation, and persulfidation.Thus, • NO and H2S are part of the crosstalk with other signal molecules such as abscisic acid (ABA), Ca 2+ , H2O2, and ethylene among others participate in the regulation of stomatal movement [53][54][55][56][57][58]. Figure 4 shows a simple model of the main signals involved in the stomata

Stomata Movement, a Process Regulated by • NO and H 2 S
Stomata are specialized cells that regulate gas exchange in the leaves and stomatal closure is one of the response mechanisms against atmospheric stress [50][51][52].It is interesting to mention that both • NO and H 2 S are molecules that, although they may be polluting molecules, are also generated endogenously by regulating stomatal closure through PTMs including tyrosine nitration, S-nitrosation, and persulfidation.Thus, • NO and H 2 S are part of the crosstalk with other signal molecules such as abscisic acid (ABA), Ca 2+ , H 2 O 2 , and ethylene among others participate in the regulation of stomatal movement [53][54][55][56][57][58]. Figure 4 shows a simple model of the main signals involved in the stomata closure where it highlights the main effect of • NO and H 2 S. Thus, • NO seems to be generated either via NR or a NOS-like activity whereas H 2 S is generated by an L-cysteine desulfhydrase (LCD) activity.NR can be inhibited by tyrosine nitration (NO 2 -Tyr) [24].On the other hand, H 2 O 2 is produced by a respiratory burst oxidase homolog (RBOH) type D/F.H 2 S triggers the generation of H 2 O 2 by persulfidation of RBOH [59] whereas it can be inhibited by S-nitrosation.• NO can inactivate the ABA receptor PYR/PYL/RCAR by a process of tyrosine nitration (NO 2 -Tyr), but • NO can also negatively regulate the open stomata 1 (OST1)/sucrose nonfermenting 1 (SNF1)-related protein kinase 2.6 (SnRK2.6)complex by S-nitrosation (Cys-NO).But SnRK2.6 can be activated by persulfidation [60,61].On the other hand, ethylene induces H 2 S production in guard cells and this H 2 S can then inhibit the synthesis of ethylene by the inhibition of 1-aminocyclopropane-1-carboxylic acid oxidase (ACO) activity by persulfidation (Cys-SSH) at Cys60 [62].

Atmospheric Pollutants and Higher Plant Response-What Happens to • NO and H2S When It Is Applied Exogenously?
At present, it is known that plants can emit • NO [11,[69][70][71] and H2S [12,72,73] to their surrounding atmosphere; however, plants could also release other gases such as CO2, nitrous oxide (N2O) [74,75] and methane (CH4) [76,77] which are part of the greenhouse gases that contribute to global warming.At the same time, it is important to note that atmospheric • NO/NOx and H2S may be adsorbed at the leaf's surface through the stomata [65,[78][79][80], and depending on their concentration, these gases can have either negative or beneficial effects on higher plants.For example, it has been pointed out that • NO Thus, it is well established that stomata movement as it has happened with photosynthesis activity can be affected by numerous atmospheric pollutants [63][64][65][66][67][68].

Atmospheric Pollutants and Higher Plant Response-What Happens to • NO and H 2 S When It Is Applied Exogenously?
At present, it is known that plants can emit • NO [11,[69][70][71] and H 2 S [12,72,73] to their surrounding atmosphere; however, plants could also release other gases such as CO 2 , nitrous oxide (N 2 O) [74,75] and methane (CH 4 ) [76,77] which are part of the greenhouse gases that contribute to global warming.At the same time, it is important to note that atmospheric • NO/NOx and H 2 S may be adsorbed at the leaf's surface through the stomata [65,[78][79][80], and depending on their concentration, these gases can have either negative or beneficial effects on higher plants.For example, it has been pointed out that • NO seems to be a key signaling molecule in the mechanism of response against higher levels of atmospheric gases including CO 2 , N 2 O, CH 4 , or O 3 which usually provoke stress in plants that have associated oxidative stress because they trigger an uncontrolled increase in the generation of ROS and RNS associated with a lower antioxidant capacity [81].Thus, the harmful or beneficial effects of the gas exchanges between plants and the surrounding atmosphere will depend on their final concentration inside the cells.
On the other hand, • NO and H 2 S as signaling molecules that are involved in numerous biological processes in higher plants, have started to be applied exogenously as alternative biotechnology tools since it has been proven that they can exert benefit effects to palliate the negative effects caused by different atmospheric factors such as high and low temperatures, O 3 , UV-B radiation or acid rain among others.

High and Low Temperature
Higher plants, during their development, are exposed to seasonal changes in temperature; consequently, they have developed the corresponding strategic adaptations that have allowed them to survive in a specific ecosystem [82][83][84].However, plants can also undergo unusual extreme temperatures provoking undesirable effects.For example, Arabidopsis thaliana exposed to heat stress (38 • C) experiences an increase in the H 2 O 2 content in chloroplasts which triggers the S-sulfenylation of the 2-phosphoglycolate phosphatase 1 at Cys86 producing its inhibition and, consequently, provoking the accumulation of 2-phosphoglycolate which has toxic effects because it inhibits the enzymes triosephosphate isomerase and phosphofructokinase which are required for CO 2 assimilation [85].In these cases, plants have to trigger a different mechanism of responses in which • NO and H 2 S, along with other regulatory molecules, participate to react and alleviate possible damages caused by extreme temperatures [86][87][88][89][90][91].
Tables 1 and 2 show some examples of how • NO and H 2 S applied exogenously can contribute to reducing the damage associated with high and low temperatures and how antioxidant systems are stimulated to alleviate oxidative damages associated with extreme temperatures.It should be mentioned that in the majority of studies in plants, the most widely used donors are sodium nitroprusside (SNP) for • NO and sodium hydrosulfide (NaHS) for H 2 S. The main reason is that both donors have a low economic cost compared to other • NO donors such as GSNO or NONOates or H 2 S donors such as GYY4137 or sulfobiotic-H 2 S donors 5a, 8ℓ, and 8o.SNP and NaHS donors are usually applied either by spraying the aerial part of the plant or by adding it to the nutrient solution.

Ozone (O 3 )
According to the predictions of Wang et al. [92], the increase in atmospheric O 3 has been estimated to be 20-25% by 2050 and it has already been proven that a high content of O 3 can negatively affect plant metabolism and growth [93][94][95] which usually triggers an increase in ROS metabolism [96,97].For example, in tobacco plants exposed to O 3 , an accumulation of • NO and H 2 O 2 was found [98].In the case of Phaseolus vulgaris, O 3 reduces the chlorophyll content and increases the content of ROS [99].Tables 1 and 2 show some representative examples of how • NO and H 2 S applied exogenously to plants can contribute to providing metabolic adaptations to high levels of atmospheric O 3 .

UV-B Radiation
UV radiation is a non-ionizing radiation that is produced by the sun and three categories of UV radiation can be distinguished according to the wavelength: 315-400 nm corresponds to UV-A, 280-315 nm to UV-B, and 100-280 nm to UV-C.UV-B radiation is the most studied in plants due to its increase on the earth's surface as a consequence of the depletion of the stratospheric O 3 layer since the atmosphere intercepts around 77% UV radiation.In this sense, plants under UV-B radiation trigger nonspecific responses such as DNA damage and an increase in ROS production as well as specific ones that involve photomorphogenic signals affecting the gene expression of UV-resistance locus 8 (UVR8) and constitutive photomorphogenesis 1 (COP1) accompanied by the transcription factor elongated hypocotyl 5 (HY5) [100][101][102][103][104].
Accumulating data indicate that in plants under UV-B radiation, the metabolism of • NO and H 2 S is exacerbated and contributes to palliating the damaged symptoms [105][106][107][108][109][110].For example, in leaves of kidney beans (Phaseolus vulgaris) exposed to UV-B stress it was found that • NO generation was associated with a NOS-like activity being mediated by H 2 O 2 [106].Additionally, the exogenous application of • NO and H 2 S has been shown to contribute at different levels to diminishing the negative impact of UV-B radiation mainly by stimulating at gene and protein levels the different antioxidant systems.Tables 1 and 2 display representative examples of how exogenous • NO and H 2 S applied can palliate the negative impact of UV-B radiation in plants.

Acid Rain
As mentioned above, acid rain is the consequence of the presence of NOx and/or SO 2 in the air during precipitation (Figure 1a).Acid rain damages plant growth since it affects photosynthesis and, in general, triggers a response of the antioxidant systems to palliate the oxidative stress [5,111,112].Some examples show that the exogenous application of several compounds such as glutathione, melatonin, or silicon could help to palliate the harmful effect on plants [113].In the model plant, Arabidopsis thaliana exposed to acid rain has been found to have an active nitrogen metabolism which has an elevated • NO production and provides a tolerance to acid rain [111].Table 1 summarizes how the exogenous • NO application modulates the plant response to acid rain.Simultaneous • NO treatment with brassinosteroids increases the leaf area, stem diameter, chlorophyll content, dry and fresh weight, and proline content.Decrease the MDA content.[116] High temperature 50 µM SNP Wheat (Triticum aestivum L.) Improve growth and photosynthetic parameters.Mitigate the oxidative stress.Increase membrane stability index.[117,118] 100 µM SNP Rice (Oryza sativa L.) • NO interacts with ethylene and H 2 S metabolism.Activation of the antioxidant system such as components of the ascorbate-glutathione cycle, accumulation of osmolytes with the concomitant increase in thermos tolerance.[119,120] Ozone (O 3 ) 50 µM SNP Arabidopsis thaliana

Conclusions and Future Perspectives
• NO and H 2 S have become paradoxical molecules in plant biology since they have gone from being hazardous molecules to becoming essential molecules in cellular metabolism, regulating physiological processes from seed germination, root development, photosynthesis, senescence, stomatal closure, formation of flowers and fruit ripening, in addition to participating in the response mechanisms against challenging environments.Paradoxically, the available information demonstrates that the exogenous application of these molecules can be biotechnological tools that allow for promoting crop resilience [137,138].In most cases, these gasotransmitters stimulate enzymatic and non-enzymatic antioxidant systems, for example, the APX activity is upregulated by S-nitrosation and persulfidation [139,140] which makes it possible to alleviate oxidative damage associated with atmospheric stressors, protecting the functionality of cells, and maintaining photosynthetic activity (Figure 5).Although we are still in the basic studies to understand the intimate molecular mechanisms exerted by • NO and H 2 S, it would be of great interest to establish protocols on how the exogenous application of these molecules can allow us to combat atmospheric stressors or other types of abiotic or biotic stresses, allowing us to connect the basic knowledge and its application to the agricultural productive sector [141,142].
Int. J. Mol.Sci.2024, 25, x FOR PEER REVIEW 9 of 14 these molecules can be biotechnological tools that allow for promoting crop resilience [137,138].In most cases, these gasotransmitters stimulate enzymatic and non-enzymatic antioxidant systems, for example, the APX activity is upregulated by S-nitrosation and persulfidation [139,140] which makes it possible to alleviate oxidative damage associated with atmospheric stressors, protecting the functionality of cells, and maintaining photosynthetic activity (Figure 5).Although we are still in the basic studies to understand the intimate molecular mechanisms exerted by • NO and H2S, it would be of great interest to establish protocols on how the exogenous application of these molecules can allow us to combat atmospheric stressors or other types of abiotic or biotic stresses, allowing us to connect the basic knowledge and its application to the agricultural productive sector [141,142].

Figure 1 .
Figure 1.Nitric oxide ( • NO) and hydrogen sulfide (H2S) participate in atmospheric pollution such as acid rain and the destruction of the ozone layer.(a) Nitrogen (N2) has a greater presence in the atmosphere but in the occurrence of atmospheric oxygen, it quickly transforms into nitrogen dioxide ( • NO2).Nitrogen oxides are acidic, and they can form nitric acid (HNO3) which can be dissolved in water, giving rise to acid rain.Similarly, H2S can also react with O2 to generate sulfur dioxide (SO2) which reacts with water droplets in clouds to create sulfuric acid (H2SO4).(b) • NO2 due to ultraviolet (UV) radiation generates • NO and atomic oxygen, which together with O2 generates ozone, which reacts with • NO, generating • NO2 and oxygen, which constitutes the photolytic cycle of the destruction of the O3 layer.

Figure 1 .
Figure 1.Nitric oxide ( • NO) and hydrogen sulfide (H 2 S) participate in atmospheric pollution such as acid rain and the destruction of the ozone layer.(a) Nitrogen (N 2 ) has a greater presence in the atmosphere but in the occurrence of atmospheric oxygen, it quickly transforms into nitrogen dioxide ( • NO 2 ).Nitrogen oxides are acidic, and they can form nitric acid (HNO 3 ) which can be dissolved in water, giving rise to acid rain.Similarly, H 2 S can also react with O 2 to generate sulfur dioxide (SO 2 ) which reacts with water droplets in clouds to create sulfuric acid (H 2 SO 4 ).(b) • NO 2 due to ultraviolet (UV) radiation generates • NO and atomic oxygen, which together with O 2 generates ozone, which reacts with • NO, generating • NO 2 and oxygen, which constitutes the photolytic cycle of the destruction of the O 3 layer.

Figure 2 .
Figure 2. Main enzymatic source of • NO and H2S in higher plant cells.(a) Nitrate reductase (NR), nitrite reductase (NiR), and L-arginine-dependent nitric oxide synthase (NOS)-like activity are the recognized major candidates for enzymatic • NO sources in the different subcellular compartments of higher plants.(b) The biosynthesis of H2S in plants is part of sulfur and cysteine metabolism which primarily involves several enzymes located in the cytosol, plastids, and mitochondria including L/D-cysteine desulfhydrase (L/D-DES), cyanoalanine synthase (CAS), serine acetyltransferase (SAT), sulfite reductase (SiR), and O-acetyl-l-serine(thiol)lyase (OASL), also named cysteine synthase.APS, adenosine 5′-phosphosulfate.Dashed line, indicates different stages.?, unidentified.

Figure 2 .
Figure 2. Main enzymatic source of • NO and H 2 S in higher plant cells.(a) Nitrate reductase (NR), nitrite reductase (NiR), and L-arginine-dependent nitric oxide synthase (NOS)-like activity are the recognized major candidates for enzymatic • NO sources in the different subcellular compartments of higher plants.(b) The biosynthesis of H 2 S in plants is part of sulfur and cysteine metabolism which primarily involves several enzymes located in the cytosol, plastids, and mitochondria including L/D-cysteine desulfhydrase (L/D-DES), cyanoalanine synthase (CAS), serine acetyltransferase (SAT), sulfite reductase (SiR), and O-acetyl-l-serine(thiol)lyase (OASL), also named cysteine synthase.APS, adenosine 5 ′ -phosphosulfate.Dashed line, indicates different stages.?, unidentified.

Figure 4 .
Figure 4. Simple model of the signaling cascade mediated by abscisic acid (ABA), H2O2, ethylene and Ca 2+ where • NO and H2S participate in the stomatal closure in response to atmospheric stresses.PP2C, protein phosphatase 2C; PYR/PYL/RCAR, pyrabactin resistance1/PYR1-like/regulatory components of ABA receptor.Red dashed lines indicate inhibitory effects.Blue dashed arrows indicate positive effects.Green dashed line, indicates blocking of activity.

Figure 4 .
Figure 4. Simple model of the signaling cascade mediated by abscisic acid (ABA), H 2 O 2 , ethylene and Ca 2+ where • NO and H 2 S participate in the stomatal closure in response to atmospheric stresses.PP2C, protein phosphatase 2C; PYR/PYL/RCAR, pyrabactin resistance1/PYR1-like/regulatory components of ABA receptor.Red dashed lines indicate inhibitory effects.Blue dashed arrows indicate positive effects.Green dashed line, indicates blocking of activity.

Figure 5 .
Figure 5. Working model of the main effects of the exogenous application of • NO or H2S under several atmospheric stressors which trigger an active ROS metabolism with the induction of antioxidant systems.

Figure 5 .
Figure 5. Working model of the main effects of the exogenous application of • NO or H 2 S under several atmospheric stressors which trigger an active ROS metabolism with the induction of antioxidant systems.

Table 1 .
Main effects of the exogenous application of • NO plants exposed to diverse atmospheric stressors.

Table 2 .
Main effects of the exogenous application of H2S plants exposed to diverse environmental stressors.