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Medrano-Macías, J.; Flores-Gallegos, A.C.; Nava-Reyna, E.; Morales, I.; Tortella, G.; Solís-Gaona, S.; Benavides-Mendoza, A. Role of RONSS on the Biostimulation of Plant. Encyclopedia. Available online: https://encyclopedia.pub/entry/44336 (accessed on 18 September 2024).
Medrano-Macías J, Flores-Gallegos AC, Nava-Reyna E, Morales I, Tortella G, Solís-Gaona S, et al. Role of RONSS on the Biostimulation of Plant. Encyclopedia. Available at: https://encyclopedia.pub/entry/44336. Accessed September 18, 2024.
Medrano-Macías, Julia, Adriana Carolina Flores-Gallegos, Erika Nava-Reyna, Isidro Morales, Gonzalo Tortella, Susana Solís-Gaona, Adalberto Benavides-Mendoza. "Role of RONSS on the Biostimulation of Plant" Encyclopedia, https://encyclopedia.pub/entry/44336 (accessed September 18, 2024).
Medrano-Macías, J., Flores-Gallegos, A.C., Nava-Reyna, E., Morales, I., Tortella, G., Solís-Gaona, S., & Benavides-Mendoza, A. (2023, May 16). Role of RONSS on the Biostimulation of Plant. In Encyclopedia. https://encyclopedia.pub/entry/44336
Medrano-Macías, Julia, et al. "Role of RONSS on the Biostimulation of Plant." Encyclopedia. Web. 16 May, 2023.
Role of RONSS on the Biostimulation of Plant
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This entry is adapted from the peer-reviewed paper 10.3390/plants11233203

Reactive oxygen species (ROS), reactive nitrogen species (RNS), and H2S-reactive sulfur species (RSS) collectively termed reactive oxygen, nitrogen, and sulfur species (RONSS), constitute a conglomerate of reactions that function as an energy dissipation mechanism, in addition to allowing environmental signals to be transduced into cellular information. This information, in the form of proteins with posttranslational modifications or signaling metabolites derived from RONSS, serves as an inducer of many processes for redoxtasis and metabolic adjustment to the changing environmental conditions to which plants are subjected. Although it is thought that the role of reactive chemical species was originally energy dissipation, during evolution they seem to form a cluster of RONSS that, in addition to dissipating excess excitation potential or reducing potential, also fulfils essential signaling functions that play a vital role in the stress acclimation of plants. Signaling occurs by synthesizing many biomolecules that modify the activity of transcription factors and through modifications in thiol groups of enzymes. The result is a series of adjustments in plants’ gene expression, biochemistry, and physiology. The action of RONSS as signaling agents in Biostimulation is discussed. 

RONSS ROS Reactive Oxygen Species Reactive Nitrogen Species Reactive Sulfur Species RNS Plant stress

1. Reactive Oxygen, Nitrogen, and Sulfur Species Integration as a Metabolic Cluster

Plant metabolism consists of a conglomerate of chemical reactions in which free energy is dissipated from physical sources such as radiation or chemical sources that store energy in chemical bonds or chemical potentials. What is obtained in organisms is metabolic energy, biomolecules, and information to maintain cellular, tissue, and organ structures in a dynamic steady state.
Cellular metabolism processes are believed to be descendants of ancient abiotic processes that dissipate free energy from physical and chemical sources, which occurred before the emergence of organized cell life [1][2][3]. Such abiotic processes should have arisen spontaneously as one of several physicochemical mechanisms through which the primordial Earth system dissipated free energy from the Sun or the stores of substances in the Earth’s crust [4][5]. It is thought that many of these processes occurred through reactions that involved the transfer of electrons [6], which could partly explain the preponderance of redox processes in the metabolism of modern organisms [7].
The goal of the above processes was to maximize entropy generation from free energy [4][8]. One way to maximize the entropy produced is to work cooperatively between different molecular species, which implies the collective organization of diverse functions in conglomerates or clusters [1][4]. It can be assumed that molecular conglomerates functioned as collaborative energy-channeling mechanisms. Different molecular complexes probably organized themselves to transfer energy from one molecular species to another, making the process of energy dissipation (or entropy generation) more effective than the result of the individual functions [9]. The chemical conglomerates or clusters were dedicated to dissipating free energy in the form of reduction potential to produce reactive chemical species such as reactive oxygen species (ROS), reactive nitrogen species (RNS), and reactive sulfur species (RSS), collectively termed reactive oxygen, nitrogen, and sulfur species (RONSS).
The cooperative work of the different components in different compartments required the creation of networks for the transmission of endogenous information that improved the ability to adjust to the conditions of the environment [1][4][10]. These information networks, including organic and inorganic soluble and volatile compounds (Figure 1), were possibly the ancestors of cell signaling processes. In Figure 1, RONSS resulting from the energy dissipation by H2S, ·NO, and inorganic and organic compounds (and lately O2) became part of the information system that monitored the energy state or redoxtasis of the different processes, regulating the joint action of the different components. In particular, the RSSH derived from the interaction of H2S with thiols could be, due to their amphiphilic nature, chemical agents that increased the system’s flexibility regarding the degrees of freedom available for the flow of electrons. Some elements such as K, Mg, Fe, Na, and Si possibly formed activation or protection systems for various system components. It is possible that some abundant elements, such as Fe and other heavy metals, have not been used in more significant volumes due to their ability to trigger oxidative reactions, which could cause system instability due to RONSS saturation. Therefore, Fe in biological organisms functions as a trace element.
Plants 11 03203 g001 550
Figure 1. Schematic representation of a prebiotic supramolecular complex that processes energy and matter [1]. The different components represented by the colored rectangles carried out specialized functions and interacted with each other coordinating through energy signals (redoxtasis) and chemical signals created by metabolites. It is possible that the RSS:RNS ratio, and later the RSS:RNS:ROS ratio, modified the redox homeostasis of the prebiotic system, modified internal signals, and caused changes in the nucleic acids, proteins, peptides, and other organic molecules of the prebiotic supramolecular complexes [11][12]. E: energy; RSS: reactive sulfur species; RNS: reactive nitrogen species; ROS: reactive oxygen species.
Compartmentalization gave rise to more sophisticated systems for copying structures, the precursors of reproduction systems, probably based on the ability to store information on functional patterns through the emergence of Hopfield-like attractor dynamics [13]. Such compartmentalization may have given rise to the first cellular organisms with different metabolic abilities, according to the energy and matter use niche in which they evolved [1].
As a consequence of the above, the metabolic processes of living organisms not only function as a mechanism to maintain the structure and functions of organisms but, as a consequence of their intrinsic dissipative nature, they still operate cooperatively to maximize the generation of entropy [8][14]. Metabolism is the set of biochemical processes that, in addition to processing matter and information, allows the acquisition, transformation, and dissipation of free energy available in the environment. Metabolism comprises a set of supramolecular conglomerates or clusters that work cooperatively, giving rise to the different phenomena that allow cellular life. The metabolic pathways that produce reactive species of certain elements, such as S (RSS), N (RNS), and O (ROS), can be an example of the above since they are linked to energy metabolism, functioning as dissipative processes of the reduction potential in excess [15][16] and can, to a certain extent, be visualized as a cluster of processes with diverse functions: the primary being energy dissipation, followed by information transfer or signaling. The dissipative processes possibly did not initially have a goal of regulating or controlling the redoxtasis but were spontaneous processes for energy dissipation. Their use as regulatory or signaling agents may be a later adaptation [17].
Other inorganic reactive species, e.g., I, Se, and P reactive species, and RONSS-derived reactive species such as lipid hydroperoxides (LOOH), carbonyl species (RCS), and malondialdehyde (MDA), have similar signaling functions [18][19][20][21][22][23]. However, they may operate at smaller concentrations than S, N, and O reactive species.
Perhaps initially with a preponderance of the RSS (H2S) and RNS (·NO) during the long Archean anoxygenic phase of planetary evolution, to later incorporate ROS [24][25], when O2 increased its concentration during the Proterozoic phase of Earth’s evolution [6][26][27]. However, if O2 or oxygen compounds such as H2O2 were present as traces before the complete oxygenic phase ([atmospheric O2] > 2%) [28], they could be sources of ROS. In the latter case, the joint evolution of the RONSS could have started before the concentration of O2 rose substantially.
The final integration and cooperation of RONSS may result, through the self-organization and creation of novelties that characterize complex systems [29], in the obtention of cooperative systems to transform free energy into information [30][31]. The information accumulated in the dynamic structures and the complexes of structures coordinated through signaling allowed the synchronization of the activities of the metabolism: first, coordinated abiotic processes, and later cellular metabolism [6][7][32][33].
Considering the abovementioned assumptions and that the different metabolic pathways for the energy dissipation and matter transformation may have formed cooperative clusters during the prebiotic era, it is to be expected that RONSS constitutes in modern organisms a system tightly coupled and coordinated with the rest of the cellular processes (Figure 2) [7][27][34]. The impact and biological functions of reactive species on plants have been extensively described in the scientific literature for ROS, RNS, and RSS individually [11][22][33][35][36][37][38][39][40][41][42][43][44]. It has been determined to a much lesser extent for the ROS–RNS, ROS–RSS, and RNS–RSS pairs [45][46][47][48][49][50][51][52][53][54][55][56] and to a lesser extent for the RONSS cluster [12][34][57][58][59][59][60][61].
Plants 11 03203 g002 550
Figure 2. Model of different energy capture and dissipation processes. Both photosynthesis and respiration, as well as the metabolism coupled with these activities, constitute dissipative mechanisms. Photosynthesis and respiration are further associated with other photochemical and biochemical energy dissipation pathways, including the production of RONSS. During the abiotic evolutionary process and later during the early biotic evolution, the production of RONSS went from being only a mechanism for the dissipation of free energy, with the consequent generation of entropy, also constituting a mechanism for regulation and transfer of information on redox and energy status between the different components of the system.

2. Reactive Oxygen, Nitrogen, and Sulfur Species as Biostimulants

From the point of view of biostimulation or priming with RONSS, the application of ROS, RNS, or RSS, or the use in pairs ROS–RNS, ROS–RSS, RNS–RSS constitutes a relevant and dynamic topic in plant science [50][57][60][61] (Table 1). In the same way, it is known that the mechanism of action of seed magnetopriming and some biostimulants, such as melatonin, salicylic acid, and silicon, includes the action of RONSS as signaling agents [62][63][64][65][66]. Although many examples are known where the application of RONSS induces favorable responses to stress, an increase in productivity or yield, or an improvement in nutritional composition in plants, there are still many gaps in knowledge about the molecular mechanisms involved in cellular responses [34][60][61]. The explanation of the above gaps lies in the great complexity of the interactions of the RONSS with the different cellular components [57][60].
Table 1. Some examples of studies where the favorable impact of applying at least two of the reactive species: ROS, RNS, and RSS or their precursors in plants has been demonstrated.
Impact on the Plant Reactive Species Plant Species Reference
Decreased absorption and/or toxicity of heavy metals H2S, ·NO
H2S, ·NO
H2S, ·NO
H2S, ·NO		 Medicago sativa
Sesamum indicum
Triticum aestivum
Triticum aestivum		 [67]
[68]
[69]
[51]
Increase in the concentration of essential elements H2S, ·NO
H2S, ·NO		 Triticum aestivum
Sesamum indicum		 [69]
[68]
Increase in Relative Growth Rate (RGR) and/or biomass H2S, ·NO
H2S, ·NO
H2S, ·NO
H2S, ·NO
H2S, ·NO
H2S, ·NO
H2O2, ·NO
H2O2, ·NO
H2O2, ·NO		 Cynodon dactylon
Medicago sativa
Sesamum indicum
Solanum lycopersicum
Triticum aestivum
Triticum aestivum
Ocimum basilicum
Oriza sativa
Triticum aestivum		 [67]
[70]
[68]
[71]
[51]
[69]
[72]
[73]
[74]
Improved crop yield and/or quality H2O2, ·NO Ocimum basilicum [72]
Increase in Relative Water Content (RWC) H2S, ·NO
H2O2, ·NO		 Triticum aestivum
Fragaria × ananassa		 [51]
[75]
Increment in stomatal conductance (gs) H2S, ·NO
H2S, ·NO		 Medicago sativa
Triticum aestivum		 [50]
[51]
Increase in the quantum efficiency of PSII (Fv/Fm) H2S, ·NO
H2S, ·NO
H2O2, ·NO
H2O2, ·NO		 Medicago sativa
Triticum aestivum
Citrus aurantium
Fragaria × ananassa		 [50]
[51]
[76]
[75]
Increase in CO2 assimilation (A) H2O2, ·NO Citrus aurantium [76]
Increment in the concentration of photosynthetic pigments H2S, ·NO
H2S, ·NO
H2O2, ·NO
H2O2, ·NO
H2O2, ·NO		 Sesamum indicum
Triticum aestivum
Citrus aurantium
Fragaria × ananassa
Ocimum basilicum		 [68]
[69]
[76]
[75]
[72]
Increased activity of antioxidant enzymes (e.g., SOD and CAT) and the ascorbate–glutathione (AsA–GSH) cycle H2S, ·NO
H2S, ·NO
H2S, ·NO
H2S, ·NO
H2S, ·NO
H2S, ·NO
H2S, ·NO
H2O2, ·NO		 Cynodon dactylon
Medicago sativa
Medicago sativa
Medicago sativa
Solanum lycopersicum
Triticum aestivum
Triticum aestivum
Ocimum basilicum		 [70]
[77]
[67]
[50]
[71]
[69]
[51]
[72]
Proteome reprogramming through reversible or irreversible posttranslational modifications (PTM) and changes in gene expression H2S, ·NO
H2S, ·NO
H2O2, ·NO		 Citrus aurantium
Citrus aurantium
Citrus aurantium		 [78]
[79]
[80]
Mitigation of the relative electrolyte leakage under stress H2S, ·NO
H2O2, ·NO
H2O2, ·NO
H2O2, ·NO		 Cynodon dactylon
Citrus aurantium
Citrus aurantium
Fragaria × ananassa		 [70]
[80]
[76]
[75]
Mitigation of lipid peroxidation under stress H2S, ·NO
H2S, ·NO
H2S, ·NO
H2S, ·NO
H2S, ·NO
H2O2, ·NO		 Cynodon dactylon
Medicago sativa
Medicago sativa
Solanum lycopersicum
Triticum aestivum
Fragaria × ananassa		 [70]
[50]
[67]
[71]
[69]
[75]
Increased accumulation of proline and other osmolytes H2S, ·NO
H2O2, ·NO		 Medicago sativa
Triticum aestivum		 [50]
[74]
Table 1 shows that coincidences occur in the proposed functions or impact on plants for the different reactive species. For example, the mitigation of electrolyte leakage and the decrease in lipid peroxidation can be achieved with the combination of ROS–RNS and RSS–RNS. Therefore, as confirmed by the studies cited in Table 4, the RONSS seems to function non-independently through crosstalk between the different signaling pathways [12][34][57][81]. The mechanism that enables the RONSS to exert their effects in a coordinated way, as explained in the first section, is thought to have been the result of prebiotic evolution that had the goal of developing processes coordinated to obtain the maximum capacity for free energy processing and entropy production [8]. The biochemical descendants of that primordial processes are still active in cells. Through billions of years of biological evolution, natural selection adjusted and adapted them to permit the maximum capacity of the cells and multicellular organisms to process free energy and transform it into entropy [10].
The purpose of maximum entropy requires that organisms have a process for obtaining information that allows them to adjust to environmental changes, which is achieved by determining the energy condition through the evaluation of the redox status of the system [82], which can be equivalent to the variations in the molar ratios of the different reactive species. Information on redox status causes changes in gene expression and phenotype adjustments and proteomic and metabolomic responses that modulate the metabolism according to the organism’s needs in a particular environment. The RONSS are relevant messengers of the above metabolic adjustments [34].
The number of known chemical agents involved in cell signaling and biostimulation will likely grow as new information about other signaling molecules that work in coordination with RONSS is acquired. H2 and CO can be examples [81][83]. RONSS work in coordination with many other biomolecules, forming an intricate network of cellular information about energy status and responses to environmental stimuli [84][85]. The preceding points to the joint use of RONSS with biostimulants such as silicon, selenium, or iodine, plant and seaweed extracts, chitosan and other biopolymers, humic substances, and metabolites such as melatonin and salicylic acid [50][62][86][87][88][89][90].
As mentioned in Table 1, the application of RONSS for signaling and as a biostimulant has been evaluated in several plants with economic purposes, such as Triticum aestivum, Solanum tuberosum, Citrus aurantium, among others, which have shown promissory results. In this regard, early studies with exogenous application of sodium hydrosulphide (SHS) as a donor of H2S on T. aestivum seedlings under Cu stress showed an improvement in the activity of glutathione reductase, dehydroascorbate reductase, L-galactono-1,4-lactone dehydrogenase and gamma-glutamyleysteine synthetase. Moreover, the levels of ascorbic acid, glutathione, and total ascorbate increased, alleviating the damage produced by Cu [91]. Reduced damage of plasma membrane integrity in T. aestivum seeds exposed to Cu, promotion of amylase and esterase activities and lower levels of malondialdehyde, and H2O2 in germinating seeds treated with H2S donors have also been reported [92]. Tolerance against Cd stress in T. aestivum through the application of NO and H2S using sodium nitroprusside (SNP) and SHS as donors, respectively, showed an increase in dry matter, chlorophyll a and b, and Fv/Fm ratio between 39.1–47.8, 61.5–92.3, and 27.2–29.1, respectively, related to the control [93]. Under cobalt (Co) stress, T. aestivum exposed to Co concentrations of 150–300 µM and treated with NO and H2S donors showed an increase of glutathione (GSH), superoxide dismutase (SOD), peroxidase (POX), monodehydroascorbate reductase (MDHAR), APX, glutathione reductase (GR), dehydroascorbate reductase (DHAR), ascorbate (tAsA), and counteracted the negative effect caused by Co on growth, water relations, redox, and antioxidant capacity in chloroplasts [51]. The addition of SNP (100 µM) as a donor of NO in T. aestivum has also been demonstrated to counteract the negatives effects of 400 µM Fe, enhanced seed germination, decreasing Fe accumulation, and proline and malondialdehyde (MDA) content [94]. Under water deficit conditions, RONSS application has also demonstrated that T. aestivum seeds can mitigate the damage produced by water scarcity. The seeds soaked with SNP (0.1 mM) or H2O2 (1 mM) or a combination of both improved Ψw, Ψs, Ψp, photosynthetic pigment content, osmolytes accumulation (GB and Pro), TSP, and the antioxidative defense mechanism. Moreover, it also reduced MDA accumulation [95].
Other species with commercial importance, such as Citrus aurantium or Solanum lycopersicum have also been evaluated. In this regard, adverse effects caused by salinity stress (120 mM NaCl) on S. lycopersicum (47% of decrease in dry leaf mass and root length) were alleviated by exogenous application of SNP (100 µM) enhanced the leaf dry mass (30%) and root length (23%) compared with the non-treated plants [96]. NO has been associated with root development in S. lycopersicum growing under elevated CO2 concentration, especially in lateral roots, and increasing nitric oxide synthase activity [97]. SNP applied as NO donor at 100 µM in S. lycopersicum showed a good capacity to immobilize As in the root but also its translocation in the shoots by upregulation of γ-glutamylcysteine synthetase (GSH1), glutathione synthetase (GSH2), phytochelatin synthase (PCS), metallothionein (MT), and ABC transporter (ABC1). Interestingly, the authors reported that the plants subjected to As stress (10 mg/L) and treated with SNP were able to restore the growth retardation through modulating the chlorophyll and proline metabolism, with an increase of stomatal conductance and NO accumulation [98]. Studies carried out with Citrus aurantium have also demonstrated how nitrosative and oxidative signals play an important role in regulating cellular adjustments to environmental conditions. In this regard, plants subjected to salinity stress (150 mM NaCl) and pre-treated with H2O2 (10 mM for 8 h) and SNP (100 µM for 48 h) showed a strong reduction of phenotypical and physiological effects, as well as a higher net photosynthetic rate compared with the non-treated plants that showed clear foliar injury (necrosis) and low net photosynthetic rates [79]. Moreover, these same authors reported that proteomics analysis reveals quantitative variations in 85 leaf proteins in plants subjected to salinity. Many of these were not present in H2O2 or SNP pre-treated plants. Histochemical and fluorescent probes in C. aurantium plants pre-treated with H2O2 and SNP showed ROS movement by vascular tissues over long distances and NO signaling pathways [76].
Strawberries are a highly demanded fruit consumed globally, known for their biological properties such as antioxidant, antimicrobial, or anti-inflammatory capacity [99]. In early studies developed with Fragaria × ananassa it was demonstrated that fumigation for 5 h with NO at 200 µL/L NO atmospheres and maintained at 18 °C in air delayed the onset of ethylene production and reduced the respiration, maintaining the fruit’s quality and prolonging its shelf life [100]. Similar results were obtained fumigating F. × ananassa with NO (between 1.0 to 4000 µL L−1) immediately after harvest and held at 5 °C and 20 °C in air containing 0.1 µL L−1 [101]. At both temperatures, the postharvest life of F. × ananassa was extended, but the optimal NO concentration was 5–10 µL L−1, causing > 50% extension in shelf life. The application of sodium hydrosulfide (NaHS) as a donor of H2S on F. × ananassa under iron deficiency has also been evaluated [102]. Leaf interveinal chlorosis caused by iron deficiency was overcome by foliar application of NaHS. Moreover, applying H2S donors enhanced chlorophyll contents and iron accumulation in young leaves. However, the H2S enhanced not only iron deficiency but also the assimilation of other micronutrients such as Zn, Ca, and Mg [103]. Iron deficiency in F. × ananassa concomitant with salinity stress (50 mM NaCl) has also been overcome by the exogenous application of NO through SNP as a donor. SNP applied at 0.1 mM showed that plants under iron deficiency and salinity reduced the exacerbated electrolyte leakage, malondialdehyde levels, and H2O2 levels caused by the stress [102]. In recent work, [104] determined that applying SNP as NO donor at 100 µM alleviated heat injury in F. × ananassa plants. NO controlled the overaccumulation of H2O2, reduced lipid peroxidation, and improved the relative water content and a higher expression of heat shock transcription factor genes involved in thermotolerance. According to the information shown above, NO or H2S are gaseous signaling molecules with an important role in response to diverse biotic and abiotic stresses in plants, regulating normal plant growth and development. This evidence suggests that RONSS are a potential tool for use in the biostimulation of crops.
The RONSS studies for their potential as signaling molecules or biostimulants have also been evaluated in medicinal plants. Although they have been less studied, medicinal plants have also been used as a model in some assays. In this regard, Catharanthus roseus, an endemic medicinal plant from Madagascar, was used as a model to evaluate its tolerance to metal stress in the presence of NO [105]. The plants were exposed to 30 mg kg−1 of Cu (CuCl2·2H2O) alone or mixed with SNP as a donor of NO in concentrations of 0–400 µM. The results showed that the damages produced by Cu in C. roseus (Cu+2 accumulation, decrease in NO production, disruption in mineral equilibrium, and high ROS production) were alleviated by SNP presence and in a more significant proportion by 50 µM of SNP. Moreover, the treatment with SNP and Cu + SNP significantly prevented or restored the Cu-induced depression of iron in the root. In addition, interestingly, the authors found that the application of SNP caused an increase in leaf vincristine and vinblastine, two potential anticancer compounds [106], which have been previously reported in C. roseus [107].
Artemisia annua is an important vegetal source against malaria [108]. Adverse effects caused by Cu+2 (20 to 40 mg kg−1) on A. annua can be alleviated by exogenous application of H2S (200 µM), restoring physiological and biochemical parameters, reducing lipid peroxidation and enhancing the antioxidant activity of plants [109]. Additionally, H2S application increased the photosynthetic efficiency and trichome density and the production of artemisinin content [108], a well-known compound used against malaria, but also with anti-inflammatory, antioxidant, and antimicrobial effects [110].
H2S has also been effectively used in Carthamus tinctorius, an Asteraceae with essential medicinal properties and a source of food-grade color in the food industry [111]. The exogenous application of H2S (1 mM) on C. tinctorius plants subjected to drought demonstrated that the harmful effects caused by the water scarcity were countered, increasing the accumulation of secondary metabolites and antioxidant capacity [112]. Exogenous application of SNP as a NO donor on Gingko biloba at different concentrations (50, 100, 250, and 500 μM) demonstrated that the high concentrations (500 μM) favored the increase of phenolic compounds, glycosides, tannins, and saponins. Moreover, a significant increase in an oxidative burst of O2− was also detected, enhanced phenylalanine ammonia-lyase (PAL) activities and antioxidant defense enzymes such as superoxide dismutase and ascorbate peroxidase [113]. Similar results were obtained in G. biloba by applying 250 μM L−1 of SNP under drought stress. The authors reported that after the treatment with SNP, remarkably soluble sugar, proline, flavonoid, and ginkgolide content was obtained in G. biloba leaves, as well as increased PAL activity, demonstrating the capacity of NO to alleviate the adverse effects caused by drought stress [114].
Another medicinal plant is Silybum marianum, which treats liver and biliary disorders. S. marianum contains silymarin, a mixture of flavonoid complexes with a protective component against drugs, including chemotherapy [115]. Field assays with two genotypes of S. marianum demonstrated that applying the SNP (100 µM) as a NO donor compensates for 40% of the adverse effects caused for drought stress, and all yield components responded significantly to treatment with SNP [116]. Applying 100 µM SNP also decreased malondialdehyde content and H2O2 in S. marianum plants submitted to water deficit and prevented a silymarin yield reduction but increased taxifolin production, silychristin, silybin, and isosilybin B [117], compounds that have been associated with the treatment of diseases due to pharmacological properties as hepatoprotective drugs [118][119]. Under drought stress applying 100 µM SNP on S. marianum, the leaf photosynthesis rate increased between 80 and 100% compared with the non-treated plants [116].
Ginsenosides are compounds associated with rhizomes and roots of Panax ginseng. It has a therapeutic potential as an adjuvant in treating diabetes mellitus [120]. In this regard, using SNP as a NO donor, together with methyl jasmonate and applied in adventitious roots of P. ginseng, has shown that a high concentration of ginsenoside was obtained with 200 µM SNP. Additionally, the application of 200 µM SNP and 100 µM methyl jasmonate caused a high induction of ginsenoside biosynthesis-related genes and detected a high sensitivity of the superoxide dismutase 1 gene [121]. In another interesting work, [122] reported stimulatory responses in Origanum majorana German type under drought stress and treated with SNP at 30 and 60 µM. Its application enhanced the growth and yield of essential oil, improved water use efficiency, and caused an upregulation in the antioxidant system. Interestingly, the use of SNP also caused a significant increase in the production of phytopharmaceuticals (total soluble phenol, anthocyanin, flavonoids, and ascorbic acid) in the herbal extract. As mentioned above, most studies have been performed under drought conditions. However, using NO has also caused stimulatory effects in medicinal plants under salt stress. In this regard, [123] developed a study to evaluate the use of NO and spermidine, a known polyamine protector of plants [124], as pretreatment of Matricaria recuita plants. The results showed increased growth parameters, significant malondialdehyde, and H2O2 content reduction, and increased ascorbate peroxidase activity.
Finally, it is essential to mention that medicinal plant extract’s biological efficacy in preventing oxidative damage is well documented [125][126][127]. However, their capacity as free radical scavenging or as biostimulant agents favoring the RONSS formation or the increase of antioxidant enzymes has been focused mainly on treating human inflammation or wounds [126][128]. On the other hand, researchers cannot ignore that plant-derived extracts can act as biostimulants in sustainable agriculture. The systematic application of plant-based products has been shown to promote plant growth and improve damage caused by environmental stresses, which has been associated with the presence of polysaccharides, polyphenols, vitamins, phytohormones, etc. [129][130]. In this regard, recent excellent reviews have focused on the role of moringa leaf as a plant biostimulant to improve the quality of agricultural products [131][132]. Hydrolysate-based biostimulants from Medicago sativa containing triacontanol and indole-3-acetic acid have been reported to stimulate the growth of Zea mays under salinity stress [133]. Since this research was focused only on RONSS species and their use as signaling molecules or biostimulant agents, this aspect will not be addressed in detail, but for more information, see [134] and [130].
NO is a labile molecule and challenging to apply in an exogenous way due to its gaseous nature and short in vivo half-life (between 1 and 5 s). NO has been successfully applied in maize to alleviate the damage produced by saline stress [135]. The authors used chitosan nanoparticles containing the NO donor S-nitroso-mercaptosuccinic acid as a carrier. As a result, a sustained NO release was reported, and amelioration of the harmful effects of salinity on the photosystem II activity, chlorophyll content, and growth of maize plants was observed [135]. In this same way, NO release from chitosan nanoparticles containing S-nitrosoglutathione (GSNO) as an NO donor was demonstrated to attenuate the effects of water deficit on sugarcane plants [136]. Furthermore, encapsulating GSNO into chitosan nanoparticles was shown to cause higher photosynthetic rates under water deficit, and increased the root/shoot ratio.
From a practical point of view, it can be thought that considering the great availability in the atmosphere and the ease of absorption of O2 by plants through stomata and lenticels, the presence of ROS in plant cells will always be ensured at the necessary quantities. The above considers the many mechanisms and environmental factors associated with ROS synthesis. However, despite the potential abundance of ROS in plant cells, different studies show that priming with ROS yields favorable results in different plant species [53][57][74].
On the other hand, unlike ROS, RNS and RSS are not obtained from a resource as abundant as O2. Instead, both RNS and RSS are synthesized from plant nutrients whose greater volume is assimilated by the root in the form of NO3−, NH4+, SO42+, and amino acids. In addition to being much smaller than those of O2 in volume, these nutrients require a previous absorption, transport, and assimilation process to produce the necessary RNS and RSS. The above implies the possibility that to obtain biostimulation with RONSS, only the exogenous application of RNS and RSS or the precursors of ·NO and H2S is necessary. It is even considered that the proper use of fertilizers with N and S can provide the amounts of RNS and RSS essential to achieving improvement in signaling and stress tolerance in plants or obtaining a more significant impact with the use of biostimulants, such as the use of elemental sulfur (S0) or organic fertilizers with S2− [137][138]. In the case of S, a regular supply of fertilizers is necessary, since repeated crop extractions and continuous land tillage that oxidizes soil organic matter cause a decrease in soil S stores [139].
A scheme similar to the one previously mentioned was presented in the study by [140], who used 100 μM ·NO (as donor sodium nitroprusside) in combination with split applications of N and S fertilizers (50 + 50 mg kg−1, two times) in plants of Brassica juncea. The results showed that the combination ·NO+N+S significantly promoted photosynthesis, stomatal performance, and growth in the absence of salt stress and meaningfully alleviated the impact of salt stress through increased proline, N- and S-use efficiency, and antioxidant system. Presumably, using ·NO in combination with the N and S fertilizer sources allowed an adequate balance of RNS and RSS.

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Subjects: Plant Sciences
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Julia Medrano-Macías
,
Adriana Carolina Flores-Gallegos
,
Erika Nava-Reyna
,
Isidro Morales
,
Gonzalo Tortella
,
Susana Solís-Gaona
,
Adalberto Benavides-Mendoza
View Times: 333
Revisions: 2 times (View History)
Update Date: 16 May 2023
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