The role of salicylic acid and gibberellin signaling in plant responses to abiotic stress with an emphasis on heavy metals

ABSTRACT

Salicylic acid (SA) and gibberellins (GAs), as two important plant growth hormones, play a key role in increasing plant tolerance to abiotic stress. They contribute to the increased plant antioxidant activities in ROS scavenging, which is related to the enzymes involved in H₂O₂-detoxifying. In photosynthetic cycles, the endogenous form of these phytohormones enhances photosynthetic properties such as stomatal conductance, net photosynthesis (PN), photosynthetic oxygen evolution, and efficiency of carboxylation. Furthermore, in cell cycle, they are able to influence division and expansion of cell growth in plants under stress, leading to increased growth of radicle cells in a meristem, and ultimately contributing to the increased germination rate and lengths of shoot and root in the stress-affected plants. In the case of crosstalk between SA and GA, exogenous GA₃ can upregulate biosynthesis of SA and consequently result in rising levels of SA, enhancing plant defense response to environmental abiotic stresses. The aim of this paper was to investigate the mechanisms related to GA and SA phytohormones in amelioration of abiotic stress, in particular, heavy metal stress.

1. Introduction

Plants are able to modify their biochemistry and physiological process in response to stressful conditions.¹ Plant hormones that are small in molecule size and exist in minute quantities in cells play pivotal roles in the regulation of plant growth processes and also plant responses to stress condition.² Among them, salicylic acid (SA; o-hydroxy benzoic acid) is one of the important plant growth regulators (PGRs) that plays a significant part in plant growth and development. SA is involved in many metabolically and physiologically important processes in plants including flowering, stomatal closure, thermogenesis,³ osmolyte metabolism, photosynthesis, fruit quality improvement, water balances, and antioxidant defense systems.^3,4 Also, SA can regulate plant photosynthetic events by impacting different parameters including stomatal closure and influencing the structure of chloroplasts and enzymes involved in photosynthesis such as Ribulose – 1,5 – BisphosphateCarboxylase/Oxygenase (RuBisCo) and carbonic anhydrase.⁵ SA is known as a phenolic phytohormone in plants that can play an important role as a signaling molecule in plants facing environmental stress.^6,7 For example, the priming of cereal seeds with SA has positive impacts on plant growth and development, which are reported in maize^8,9 and also in rice.^10–12 Therefore, SA can lead to improving biological, physiological, and morphological indexes in plants as well as yield components.⁸ This has also been shown by pre-soaking seeds by application of SA in young leaves of maize seedlings, leading to the enhanced superoxide dismutase in the plant.⁵ On the other hand, increasing photosynthesis and grain yield are reported to be among many other positive impacts of seed priming with SA application.¹² But an important aspect of SA is increasing polyamine contents in seeds exposed to priming with different quantities of SA, which can result in the acclimatization of plants under stress.¹² SA plays a positive role in ion channels regulation, photosynthesis cycles and can increase antioxidant enzymes and defense mechanism in plants.¹³ It is reported that seed priming with SA is more effective than SA foliar application.⁸ However, the foliar application of SA can improve seed germination by increasing chlorophyll biosynthesis and bioactive compounds contents such as polyphenols and betacyanins. SA has the ability to increase antioxidant activities in plants under stress conditions.¹⁴ Gibberellins (Gas), as an important phytohormone, belongs to tetracyclic diterpenoid carboxylic acid groups.¹⁵ GAs can induce growth and development process in plants including promoting seed germination, flowering, fruit ripening, leaf expansion, and preventing the development of trichome.¹⁵ They act as small plant growth molecules influencing growth and development in entire plant life cycle. GAs play an essential role in increasing cell elongation and cell division and are also involved in the development of transition phases. They play a part in triggering seed development processes such as seed germination and release of seed dormancy, adult and juvenile growth phases, where seedlings without the ability to perceive or synthesize GAs develop into plants with retarded growth.^16,17 GAs are involved in plant mechanisms associated with enhanced resistance under abiotic stress, which is characterized by promoting plant growth and development in stress condition.² In a study, it was shown that GA₃ (as the most active gibberellin) increased plant adaptation to the low level of heavy metals of lead (Pb) cadmium (Cd) in green algae Chlorella Vulgaris (Chlorophyceae).¹⁸ Also, in maize, GA₃ improves seed germination and establishment under metal stress conditions through enhancing the efficiency of membrane permeability and improving nutrient levels.¹⁹ Besides, GAs have an important role in the regulation of sink-source transfer rate under different growth conditions so it can adjust assimilates translocation with some mechanisms such as changing sink and source formation, regulation of resource mobilization and elevating photosynthetic rates.²⁰ In the case of cell cycle, GAs have the ability to keep cell integrity and preserve cell division, which has been documented in an experiment on C.Vulgari exposed to metal toxicity (Pb and Cd) in which GA₃ protected cellular division process.²¹ Generally, GAs can improve plant detoxification mechanisms against heavy metal stress with the activation of different defensive lines, synthesis of catalase, and accumulation of phytochelatins.²² Below we consider the mechanisms associated with these two phytohormones (salicylic acid and gibberellin), which are assumed to be involved in increasing abiotic stress tolerance, particularly, metal stress in plants and also investigate their detoxification ability in plants subjected to heavy metal stress. Then, in the last topic, we survey the possibility of interaction between salicylic acid and gibbering under heavy metal stress.

2. Salicylic acid (SA) as a phytohormone against heavy metal stress

SA, as an endogenous plant hormone, can improve plant growth process and also can raise plant resistance under osmotic or ozone stress by mechanisms such as the production of some stress proteins.²³ Also, SA can increase the efficiency of fluorescence process and regulate transpiration and prevent ethylene synthesis, and also can enhance plant resistance to various pathogenic diseases.²³ Many researchers have proved that SA can ameliorate heavy metal stress in many plant species,^24,25 which has been reported for Hg in alfalfa and Medicago sativa,²⁶ Pb in pea and Indian mustard,^27,28 and Cd in Thlaspi and maize.^29,30 SA, as a biochemical factor, has a positive role in increasing plant tolerance to heavy metal stress³¹ so that SA has a special capacity to counteract toxicity arising from heavy metal stress by the disintegration of ROS (Reactive Oxygen Species),⁵ which is associated with localization of heavy metal parts in cellular compartments.^32,33 Exogenously applied SA elevates the resistance of the plant to heavy metal stress through the activation of production of antioxidant enzymes which results in lowered levels of ROS.^23,34 It is shown that CAT and SOD activities in barley under heavy metal stress were increased by SA.²³ Likewise, in Linum usitatissimum L. exposed to Cd, SA has been shown to play an important role in increasing antioxidant activities and related enzymes involved in H₂O₂-detoxifying, leading to the inhibition of oxidative stress caused by Cd in the plant.³⁵ Exogenously applied SA is reported to be involved in reducing the damaging effect of Cd on plant cells,³⁶ which indicates the signaling pathways network between exogenous SA and heavy metal stress.³⁷ Some studies have reported that SA can assume the role of an iron-chelation molecule or can directly act as a scavenger of hydroxyl radicals and degrade metal-bioactivity by enhancing antioxidant enzyme activities.³⁸ On the other hand, proline can have a major role in the stimulation of antioxidant, which can result in increased antioxidant activities similar to an osmolyte in plants under stress condition.^32,33 Oxidative stress caused by ROS products such as H₂O₂ can be reduced by optimal concentrations of SA. In plants, when H₂O₂ is accumulated in high concentration, toxicity in plants caused by the production of reactive hydroxyl radicals can lead to oxidative stress and eventually disturb plant metabolism.³⁵ But, the low concentration of SA can improve plant tolerance and increase plant defense mechanism by inducing antioxidant enzyme activities, leading to reduced oxidative stress.^35,39 Phytohormones regulate plant growth and development under heavy metal stress.⁴⁰ The positive impact of exogenous SA on heavy metals has been reported by many studies which often cite the important role of exogenous SA in terms of increasing antioxidant activities in scavenging ROS.^41–44 However, some of the studies have reported that SA leads to decreasing CAT activity as an antioxidant enzyme in the plant under metal stress.^45,46 This reduction in CAT activity is attributed to increasing levels of H₂O₂ in plant and augmented peroxidase activity. One reason for this process is the act of H₂O₂ as a secondary messenger that triggers signaling cascades, which can stimulate and increase defensive activities in plants under moderate stress.^26,47 SA can influence plant physiology and morphology under heavy metal stress. In one study, it was shown that increasing cadmium influenced plant shoot/root ratio and decreased rate of shoot/root, but the low concentration of SA elevated the rate of shoot/root via increasing chlorophyll levels in the plant under Cd stress.³⁵ Therefore, exogenous SA can increase chlorophyll content in plants subjected to heavy metal stress, which has been confirmed by the different studies using different plants.^48,49 SA can impact division and expansion of cell growth cycles and increase the growth of radicle cells in meristem which leads to increasing germination rate and lengths of shoot and root in plants.⁵⁰ In an experiment with rice exposed to salt stress, it was shown that SA as a regulator ameliorated the adverse effect of salt stress so that SA reduced the concentrations of Na+ and Clˉ ions caused by salt stress in rice by influencing biomolecule structures and transport of K+ in the cell.⁵¹ SA can improve seed germination and increase seed growth in rice under Pb²⁺ or Hg²⁺ stress.⁵² In the case of plant nutrient, many researchers have shown that mineral nutrients have an essential function in the amelioration of heavy metal stress in plants.^20,53 SA plays an important part in absorption, uptake, regulation of mineral nutrients, contributing to the maintenance of the integrity of cellular membrane, which can improve plant growth and development under abiotic stress.^54–56 Nevertheless, SA may have some adverse effects on plants. This depends upon its concentration, plant species, and the mode of application. So it can have either damaging or protective effect on plants under heavy metal stress.⁵⁷ Under abnormal conditions, such as the application of extreme doses of SA, it can lead to the accumulation of hydrogen peroxide and consequently generate oxidative stress in plants.⁵⁸ In a study on Arabidopsis thaliana, it was shown that SA induced production of ROS in photosynthetic tissues when the plant was subjected to salt stress and osmotic condition.⁵⁹ Generally, various factors contribute to SA efficiency in plants coping with heavy metal stress. Experiments under controlled or changing climate conditions can give different results. Also, results may be different in cultured condition for example in vitro or hydroponic or on the farm. The concentration of SA is very important in determining the impact of SA under stress condition so that high level of SA may be harmful to plant and can lead to a deleterious impact on plant growth and development.⁶⁰ Many studies have reported that the moderate levels of SA can elevate plant resistance under heavy metal stress, which is reported in maize and pea plants under Cd stress.^47,61,62 There is a specified SA concentration in various plants which can be in the range from 1 microgram/gram fresh weigh in maize, wheat, and tobacco under normal growth conditions to 30–40 microgram/gram in rice and thermogenic plants.⁶³ In general, SA can alleviate heavy metal stress in plants by four metabolic pathways including metal-chelating compounds, antioxidative defense systems, osmolytes, and secondary metabolism.⁵ In the case of antioxidant pathways, SA as a small signaling molecules can play an essential role in systemic acquired resistance (SAR), which is involved in signaling responses to abiotic stress, leading to activation of plant defense mechanisms including stimulated expression of the genes related to antioxidant activity and modulation of cellular redox homeostasis and alteration in transcription element activities. In this way, SA through signaling pathways networks is involved in non-expression of PR-protein 1 (NPR 1), which is related to redox-regulated protein in plants.⁶⁴ Therefore, elevated endogenous SA levels can lead to the stimulation of expression of PR genes and improvement of SAR in plants.⁶⁴ In fact, SA in plants encountering heavy metal stress increases plant resistance via activation of some regulators of plant immune system including NPR 1a, NPR 3and NPR 4, which can act as SA receptors.^65,66 Generally, SA synthesis in plants under heavy metal stress is made possible by two pathways; the first one is related to phenylalanine pathways in which phenylalanine ammonia-lyase converts phenylalanine to cinnamic acid and can regulate phenylpropanoid pathways and occurs by biotic and abiotic processes in plants.⁶⁷ Cinnamate-4-hydroxylase and phenylalanine ammonia-lyase are the two essential enzymes in phenylpropanoid pathways and it is shown that methyl salicylate and methyl Jasmonate increase transcription of the gene and enzymatic activities involved in the formation of these two enzymes in rice plant, leading to accumulation of phenolics in rice.⁶⁸ The phenylalanine pathways are also involved in the production of metabolites such as lignans, flavonoids, and coumarins. Another pathway to synthesis of SA is by chorismate via isochorismate where SA synthesis occurs in chloroplasts by the enzymes of isochorismate pyruvate lyase and isochorismate synesthetes.⁶⁹ In the case of metal-chelating compounds, SA can play an important role in the formation of proteins involved in metal-chelating compounds. PCs and MTs are two important metal-chelators, which have the ability to bind with metal ions and can scavenge and ameliorate metal stress in plants. Also, sulfur and glutathione are of the important compounds in these two pathways. SA via enhancing sulfur and glutathione assimilation and total none-protein thiol content can increase quantities of PCs and MTs and eventually improve metal chelation in plants under heavy metal stress.⁵ This phenomenon is reported by some studies.^26,29 Secondary metabolites, although not required for plant survival, play an important role in increasing plant resistance against abiotic stress.⁵ They are considered to be the primary source of flavors or additives of food and are deemed to be a pathway involved in the amelioration of heavy metals in plants by SA.⁷⁰ The levels of SA can increase secondary metabolite contents in plants under heavy metal stress, which can help the plant to improve resistance against metal stress.^5,71 This has been reported by many studies with different heavy metal-stressed plants in which SA increased the concentration of secondary metabolites such as PAL content and total soluble phenols in Matricaria chamomilla plants under Cd and Ni stress,⁷² protocatechuic acid and aldehyde in scenedesmus quadricauda plant under Cu stress,⁷³ beta-carboline alkaloids content in Zygophyllum fabago under Pb stress.⁷⁴ In the case of osmolyte stress mitigating mechanisms, plants first need to maintain osmotic balance and cell integrity. This is achieved by osmoregulatory factors, which can preserve cell turgor in stress condition. The osmoregulation is assisted by some mediators such as glycinebetaine, proline, and soluble sugars.⁷⁵ Glycinebetaine is one of the important compounds in plants when it comes to coping with osmolyte and heavy metal stress and has a strong ability to reduce osmotic stress in the cell.^76,77 It can act as a mediatory compound to protect cellular membrane integrity, to maintain osmotic balance, to detoxify metal, and to preserve RuBisco activity in heavy metal–affected cells.³² SA can interact with glycine betaine and increase plant defense mechanism against osmolyte and heavy metal stress.⁷⁸ Proline is another mediatory compound in osmolyte pathways. Accumulation of proline can lead to amelioration of heavy metal stress by scavenging ROS compounds, maintaining essential enzymes equilibrium, increasing content of proteins involved in plant defense mechanism systems, protecting cell membranes, and regulating osmotic balance in plant cells.⁷⁹ SA can influence enzymatic activities involved in proline biosynthesis including pyrroline-5- carboxylate reductase and Ỹ- glutamyl kinase. SA can also ameliorate proline oxidative process, leading to increased proline content and consequently raising plant defense capability under heavy metal stress.⁷⁸ The increase in proline content by salicylic acid is reported by Shakirova et al., (2003) in wheat seedlings.⁸⁰ Also, increasing soluble sugars and polysaccharide contents by application of SA is reported by^81,82 which act as an osmo-protectant agent, elevating plant tolerance under osmotic and metal stress. In photosynthetic process, SA can improve photosynthesis indexes including stomatal closure, rubisco activity, accumulation of photosynthetic pigments as well as the structure of chloroplast.^83,84 SA can be a regulator of photosynthetic activities and a preserver of redox homeostasis.⁸⁵ Many studies have reported that SA can play an ameliorative role in plant photosynthesis under stress condition and can improve photosynthetic efficiency.^53,86-88 SA has been shown to directly influence stomatal closure with the regulation of PSII-ETC, but it influences PSII in stress-affected plants in an indirect manner.⁸⁹ These studies show that SA can improve plant resistance under abiotic stresses such as drought, heat and especially metal stress by improving photosynthesis indexes, reducing PSII damage, regulating the distribution of assimilates and PSII electron transport, increasing PN and photosynthetic pigments, activating rubisco, and increasing ROS-scavenging enzymes as well as enhancing membrane integrity.⁹⁰

3. Gibberellins (GAs) as phytohormones against heavy metal stress

The gibberellins (GAs) often exist in GA₁ and GA₃ forms. They belong to the tetracyclic diterpenoid carboxylic acids. However, many of them are not considered as effective hormone for plant growth and development but the small part of their function can play crucial roles in plant growth and developmental stages,⁹¹ which include flower and fruit development, stem elongation, leaf expansion, and trichome initiation¹⁵ and plant important cycles related to growth functions and transition phase.² GAs can affect plant osmotic response, which is shown in Arabidopsis thaliana.^92,93 There are several pathways in gibberellin signaling including F-box protein GID2/SLEEPY 1 (SLY1),⁹⁴ GID1 receptor,¹⁷ and transcriptional regulator via DELLA proteins.⁹⁵ So that GAs can bind to the GID1 receptor, which is a prelude for the initiation of interactions with DELLA proteins, which acts as negative regulators in signaling pathways. Therefore, after the formation of this complex, DELLA proteins are degraded by the 26 S proteasome where the DELLA protein GID2/SLY1 interactions play a mediatory role in this process, which is implicated in GAs responses.⁹⁶ GAs biosynthesize occurs in plastids with forms of trans-geranyl diphosphate through pathways of methylerythritol phosphate,⁹⁷ which is oxidized by 2-oxoglutarate-dependent dioxygenases and cytochrome P450 monooxygenases in endoplasmic reticulum in plastids.⁹⁸ However, GAs biosynthesis through signal development in dioxygenases site takes place with the genes encoding dioxygenases. It is shown that a group of genes are involved in GAs biosynthesis pathways which include GA20ox (GA 20-oxidase), GA3ox (GA3-oxidase), and GA2ox (GA2-oxidase). Among them, GA2ox is involved in plant responses to abiotic stress.^2,99 It is reported that abiotic stress decreases GAs content by the regulatory role of GA2ox genes which is cited as a general hypothesis related to this gene in the regulations of GAs in stress condition. However, in some cases, the down-regulatory role of GA2ox genes in stress conditions is reported.² On the other hand, the investigation into GAs signal transduction has led to the identification of one of the most important signaling components,¹⁰⁰ which is called DELLA and categorized as a nuclear protein and a transcriptional regulator in GRAS family, which plays a suppressor role in GA-related signals.¹⁰¹ GAs role in plant growth regulation in the face of many kinds of abiotic stress is mediated by DELLA.^102,103 Exogenous application of GA has been associated with concurrent accumulation of DELLA, which is reported in A.Thaliana under salt stress condition, revealing a link between DELLA function and salt stress.^103,104 This is indicative of the essential role of DELLA in enhancing plant tolerance under stress conditions,^105,106 which occurs in transgenic lines of pRGA: GFP-RGA with gene expression of GFP-RGA fusion protein exposed to high levels of salt stress, leading to increased signal by GFP-RGA.¹⁰⁴ In an investigation on A.Thalina by Achared et al., (2008), it was reported that transcriptional regulation by DELLA is involved in regulation and induction of plant antioxidant defense system.¹⁰⁵ Therefore, it can be stated that DELLA responses to stress are associated with a reduction in ROS accumulation, which can delay the onset of cell death brought on by ROS compounds in plants under stress.¹⁰⁵ On the other hand, DELLA influences the regulation of cellular processes such as cell expansion and cell proliferation in stress condition.¹⁰⁷ This is shown in A.thalinia where DELLA activity and cell number are reported to significantly decrease even in wild-type plants.⁹³ However, in stress condition, DELLA enhances the expression of proteins involved in cell cycle inhibition including SIAMESE (SIM) AND Kip-related protein 2(KRP2), which is effective for plant cell surviving and is an acclimatization strategy by most plants coping with stress conditions.¹⁰⁷ Nevertheless, DELLA mechanisms in the face of stress condition are poorly understood. In other instances, it was shown that GA could ameliorate the adverse effects of Cd and Pb on yield and biochemical processes of Vicia faba by GA₃ mediation. So that it is reported that GAs can increase mitotic activity (the indexes of cell division) and some biochemical and metabolism process in Vicia faba L. plants under two heavy metals (Cd and Pb) stress, positively influencing yield and seeding growth of the plant.¹⁰⁸ In some studies, it is indicated that GA₃ bioactivity was decreased in the treatments in which plants were exposed to Cu, leading to the promotion of plant growth. This shows the role of GA biosynthesis in the alleviation of heavy metal stress.^109,110 GA₃ has the ability to increase the content of endogenous amino acid in plants,¹¹¹ which can influence plant metabolism processes such as regulation of membrane permeability, enzymatic activities, osmolytes, ion uptake, leading to enhanced plant tolerance to abiotic stress.¹¹² Also, it can improve photosynthetic efficiency and nitrogen fixation.¹¹¹ The evaluation of GAs impact on photosynthesis in plants under abiotic stress is one of the important aspects of GAs ability in terms of plant cell detoxification. It is reported that the application of exogenous GA₃ on broad bean and soybean can enhance photosynthetic properties such as stomatal conductance, PN, photosynthetic oxygen evolution, and efficiency of carboxylation.¹¹³ Also, in another study investigating seeds of wheat under salt stress, GA₃ treatment increased photosynthetic indexes of PN, water-use efficiency, transpiration rate, and stomatal conductance.¹¹⁴ In maize under high concentration of salinity, it was shown that the application of GA improved accumulation of chlorophyll and proline, and enhanced activity of the enzymes involved in ROS-scavenging.¹⁹ This can be related to the increasing levels of special enzymes involved in the regulation of photosynthetic carbon fixation (ribulose-1,5-bisphosphate carboxylase (RuBPCase)).⁹⁰ Many studies have reported that GAs can raise plant tolerance to heavy metal stress through improving photosynthetic activities.^115–117 This has been shown in sunflower exposed to Cu stress where GAs treatment enhanced trapping of energy in PSII reaction centers, and increased LHCII complex stability, PN, and Fv/Fm.¹¹⁵ Also, GAs are reported to increase rate of growth, chlorophyll content, and net CO₂ assimilation rate in soybean under Cd stress.¹¹⁶

4. Cross talk between gibberellin (GA) and salicylic acid (SA) under heavy metal stress

Some researchers have reported the interaction between GA and SA in both normal and stressful conditions.^118,119 Gibberellin and salicylic acid participate in the regulation of numerous plant responses. They are implicated in the stimulation of protein expression involved in pathogenesis.³ Moreover, they interact with one another to improve plant defense mechanism under abiotic stress.^120,121 SA increases plant tolerance under abiotic stress.⁵⁷ It has the ability to increase antioxidant activities and decrease lipid peroxidation.¹²² The results obtained by Arabidopsis seedling exposed to SA under salt stress indicate that SA through the stimulation of the production of two superoxide dismutases, improves seed germination and increases antioxidant capacity, enhancing the plant tolerance to salt stress.¹²³ Under stressful conditions, GA-SA can interact as a functional compound to elevate plant resistance against abiotic stress.¹²⁴ This is mediated by the GA–induced genes.¹²⁵ It is shown that FaGASA4 transgenic line in Arabidopsis is much resistant to abiotic stress such as oxidative and salt stress¹²⁶ so that the inoculation of Arabidopsis seeds with 50 μM GA₃ for 24 h resulted in 2-fold SA levels increase as compared to seeds incubation in water and wild-type of the plants.¹²⁶ So that the stimulated enhancement of gene expression of NPR1 (nonexpressor of PR-1), and the ICS1 (isochorismate synthase), which are involved in the biosynthesis of SA and its perception and are implicated in overexpression of FcGASA4, can increase SA content in seeds during germination as compared to their wild-type counterparts.¹²⁶ Exogenous GA₃ can upregulate biosynthesis of SA and with rising levels of SA, and as a result, plant defense response to abiotic stress is enhanced.¹²⁶ So that when seedlings with gene FaGASA4 are grown in GA₃ medium, ics1 and npr1 genes are expressed, which are the main exogenous factors in biosynthesis and action of SA,¹²⁶ preventing the adverse impact of abiotic stress on seed germination.¹²⁶ Therefore, the interaction between SA and GA (SA-GA) has the ability to ameliorate abiotic stress by induction of SA biosynthesis and consequently increase plant tolerance under abiotic stress, which is modulated through GA-SA intermediate genes.¹²⁷ A schematic diagram of this is given in Figure 1. On the other hand, isocitrate lyase enzyme, which is an essential enzyme in lipid metabolism during seed germination,^128,129 is reported to be influenced by SA in Arabidopsis thaliana during seed germination.¹²³ On the other hand, the enhancement of endogenous SA levels occurs after exogenous application of GA₃ which is related to GA-induced overexpression of GASA4 gene.^118,126 So GAs are involved in the stimulation of isocitrate lyase gene expression by influencing SA biosynthesis, and action.¹²³ Therefore, it can be stated that GA influences seed germination and growth process under abiotic stress conditions,¹¹⁸ which is modulated by cross talk between salicylic acid and gibberellin.

Figure 1.

Cross talk between exogenous GA (giggerellin) and SA (Salicylic acid) under abiotic stress.

5. Conclusion

Salicylic acid (SA) is one of the important plant growth regulators (PGRs) and plays a positive role in plant growth and development. It can participate in plant growth processes such as flowering, fruit quality improvement, water balances, stomatal closure, photosynthesis, as well as antioxidant defense systems. It can increase plant resistance under stress with the activation of some mechanisms, such as producing some stress proteins, regulating transpiration and improving efficiency of fluorescence process and inhibiting ethylene synthesis. Many researchers have reported the role of SA in the reduction of metal toxicity. SA can counteract toxicity arising from heavy metal stress and disintegrate ROS. SA increases plant resistance and tolerance to abiotic stress by increasing antioxidant activities and related enzymes involved in H₂O₂-detoxifying. In terms of growth attributes, the evidence indicates that the low rate of shoot/root is elevated by a low concentration of SA along with increasing chlorophyll levels in the plants under Cd stress. Also, the exogenous application of SA can increase chlorophyll contents during plant growth under heavy metal stress. Also, in cell cycles, SA influences cell elongation, cell division, and cell expansion of growth cycles, leading to enhanced growth of radicle cells in meristem, which in turn, leads to increased germination rate and enhanced shoot and root growth in heavy metal-stressed plants. In terms of mineral elements, SA plays an important role in absorption, uptake, regulation and maintaining integrity of membrane, improving plant growth and development under abiotic stress. Generally, there are four main metabolic pathways in SA to make it possible for plant to cope with heavy metal stress which include metal-chelating compounds, antioxidative defense systems, osmolytes, and secondary metabolism. Gibberellins (GAs) are involved in many plant life processes such as those related to plant development and plant response to stress. They play a pivotal role in the transition phases involved in plant growth and development such as seed germination, seed dormancy, adult and juvenile growth phases, flowering, and fruit ripening. They play an essential role in increasing cell elongation and cell division. Also, there are several pieces of evidence indicating that GAs are involved in raising plant tolerance to different abiotic stresses. It is reported that the defense response of GAs under abiotic stress includes reduction of GA levels via increasing accumulations of DELLA proteins. On the other hand, GA₃ enhances the content of endogenous amino acid in plant, which can result in enhanced plant tolerance to abiotic stress by increasing plant metabolism processes such as regulation of membrane permeability, enzymatic activities, osmolytes, and ion uptake. The other GA-mediated mechanism in terms of increasing plant tolerance to metal stress is related to enhancement in photosynthetic efficiency. Therefore, GAs can increase photosynthetic properties in plants under abiotic stress such as PN, water-use efficiency, transpiration rate, and stomatal conductance. Moreover, GAs improve the accumulation of chlorophyll, proline, and enhance the activity of the enzymes involved in ROS-scavenging. There is an interaction between gibberellin and salicylic acid under both normal and stressful growing condition. The cross talk between SA and GA has been shown in Arabidopsis, which involves the regulatory role of GAs in SA biosynthesis. The expression of responsive genes of GA additionally raises endogenous levels of SA. SA induces plant tolerance under abiotic stress. It has the ability to increase plant antioxidant activities and decrease lipid peroxidation. Under stressful conditions, GA-SA interacts as a functional compound, elevating plant tolerance to abiotic stress, which is mediated by the GA-induced genes. This indicates the impact of GA-SA cross talk in improving plant resistance under stress conditions. In general, SA and GA, as two important plant growth phytohormones, are the key regulators for increasing plant tolerance to abiotic stress, which is achieved by some pathways involved in plant defense mechanisms including stimulated expression of the genes associated with antioxidant activity, modulation of cellular redox homeostasis and alteration in transcription element activities.

Funding Statement

This work was supported by the financial funds provided by Nanjing Forestry University (Start-Up Research Fund) and Bamboo Research Institute for the current study. Special Fund for this work was supported by National Key Research & Development Program of China (Integration and Demonstration of Valued & Efficiency –increased Technology across the Industry Chain For bamboo, 2016 YFD0600901).

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.