Interaction of sulfur with phytohormones and signaling molecules in conferring abiotic stress tolerance to plants

ABSTRACT

Sulfur (S) is a macronutrient for the plant, which has an immense role in basic plant processes and regulation of several metabolic pathways. It has also a major role in providing protection against adverse conditions. Sulfur-containing amino acids and metabolites maintain plant cell mechanisms to improve stress tolerance. It interacts with several biomolecules such as phytohormones, polyamines, nitric oxide (NO), and even with other plant nutrients, which can produce some derivatives those are essential for abiotic stress tolerance. Different S derivatives stimulate signaling cascades, for the upregulation of different cellular messengers such as abscisic acid, Ca²⁺, and NO. Sulfur is also known to interact with some essential plant nutrients by influencing their uptake and transport, hence, confers nutrient homeostasis efficiencies. This review focuses on how S is interacted with several signaling molecules like NO, glutathiones, phytohormones, hydrogen sulfide, polyamines, etc. This is a concise summary aimed at guiding the researchers to study S-related plant processes in the light of abiotic stress tolerance.

Keywords:

• cysteine
• glutathione
• nitric oxide
• phytohormones
• ROS
• stress signaling

As a sessile organism, the plant faces various obstacles in acclimation and adaptation to the surrounding environment.¹ The role of plant nutrients in plant abiotic stress is well known. Although sulfur (S) is the fourth major nutrients, it plays a vital role in regulating many foremost plant processes. There are some sporadic research findings confirmed about signaling function of S and its derivatives such as glutathione (GSH), hydrogen sulfide (H₂S), methionine (Met), cysteine (Cys), phytochelatin (PC), ATP sulfurylase (ATPS), protein thiols, etc.² Sulfur and its derivatives have been reported to improve the antioxidant defense to scavenge excessive reactive oxygen species (ROS) under different abiotic stresses. In presence of S, the GSH content, ratio of GSH and glutathione disulfide, GSSG (GSH/GSSG), non-protein thiols (NPTs) and PCs, ascorbate (AsA) content, ratio of AsA and dehydroascorbate, DHA (AsA/DHA), activities of AsA peroxidase (APX), GSH reductase (GR), catalase (CAT) were improved in Cd affected Brassica juncea. Moreover, superoxide dismutase (SOD) expression was upregulated that decreased superoxide radicals (O₂^•−).³ Sulfur addition decreased the As uptake and content in the shoot, modulated thiol metabolism, glycolysis and amino acid in Oryza sativa.⁴ Apart from the direct effect, the interaction of S with other molecules is very common to counteract abiotic stress. Sulfur can interact with different phytohormones including auxins (AUX), gibberellins (GA), cytokinins (CK), abscisic acid (ABA), ethylene (ET), jasmonic acid (JA) and salicylic acid (SA) under abiotic stress situation, and positively regulates plant defense⁵ (Figure 1). Sulfur contributes to improving stress tolerance by interacting with some other plant nutrients. Some S derivatives like H₂S involved in a complex signaling network consisting of many secondary messengers and phytohormones such as Ca²⁺, ABA, hydrogen peroxide (H₂O₂), nitric oxide (NO), and polyamines (PAs), which protect the plants from stress-induced damages⁶ (Figure 1). Recently, reactive S species (RSS), a group of S-related free radicals have been designated, which modulate the redox status of biological thiols and disulfides, hence positively act to confer stress tolerance.⁷ Therefore, it is necessary to extend research with S to exploit its function thoroughly. In this review, we present a brief overview of the interaction between S and other cellular molecules in enhancing abiotic stress tolerance based on the recent available literature.

Figure 1. Interaction of S with phytohormones and other signaling molecules in the signaling cascade to combat abiotic stresses. Here, GSH plays a central role which interacts with NO and produce GSNO to provide signal. GSH is also actively involved in metal chelation and also regulates antioxidant defense system. NO is directly interacted with H₂S which further modulates several molecules and their functions. Cysteine is one of the major S-containing amino acids which is interacted with several phytohormones and also regulates PAs and other molecules via several pathways. Dotted lines represent activation or enhancement. Additional details are in text.

Sulfur is associated with phytohormones regulation

Although phytohormones influence metabolism of S, some phytohormone require S or its derivative compounds for their biosynthesis. The greatest instance is the ET, and the biosynthesis of ET is evidently reliant on S bioavailability and firmly connected with Met metabolism.⁸ At the beginning Met activated to form S-adenosylmethionine (SAM), which transformed to 1-aminocyclopropane carboxylate (ACC). This ACC is used as the substrate for ethylene biosynthesis. On the other hand, the co-product from ACC biosynthesis —5-methylthioadenosine, is further recycled back to Met and serve as the source of S to plants.⁹ Sulfate (SO₄²⁻) deficiency to plants not only reduces the SAM levels but also disrupts the ethylene and ABA formation; leads to lower Cys synthesis rate, in turns lower levels of ABA, and poor abiotic stress tolerance.¹⁰ Therefore, efficient S metabolism is urgent for biosynthesis of at least some of the phytohormones such as AUX and indole 3-acetic acid (IAA).^11,12 For instance, decrease in GSH levels in the cell results in a sharp decline of AUX gradient in root tips and showed alteration of lateral root growth and density.¹² Although, CK levels declined in SO₄²⁻ deficit plant leaves this hormone is not linked directly to the response of S starvation, rather regulates SO₄²⁻ uptake and metabolism. Moreover, CK receptor – CRE1 and CK act similarly in SO₄²⁻ uptake and regulation.¹³

In plants, JA or its derivatives induce sulfide formation, GSH biosynthesis, and glucosinolate (GS) metabolism without altering the steady state of Cys or GSH, but accumulate GSs.¹⁴ Some transcription factors also responsible for controlling JA responses, namely MYC2, MYC3, and MYC4, also controls GS synthesis.¹⁵ Sulfur yet again had some role in JA signaling via 12-oxo-phytodienoic acid (OPDA) and cyclophilin CYP20-3 JA precursors. For producing O-acetyl serine (OAS), the precursor of Cyt, OPDA-CYP20-3 complex interacts with serine acetyltransferase (SAT), and to accomplish this mechanism S metabolites are necessary.¹⁶ On the other hand, 3ʹ-Phosphoadenosine-5ʹ-phosphosulfate (PAP) is also responsible for signaling S metabolism during drought stress.¹⁷

Both ET generation and S metabolism path shares several metabolites. Assimilation of SO₄²⁻ during salt stress revealed that APS reductase activity is upregulated by exogenous application of ET precursor ACC, which increased transcription of APR1 and APR3 genes.¹⁸ Methionine is a precursor of ET, and that cease ET biosynthesis. Methionine pathway also contributes to the metabolism of ET and S¹⁹ by SAM, which is also an ET precursor. Mao et al.²⁰ reported that FERONIA, a plasma membrane receptor-like kinase, is involved in regulation of SAM. Moreover, reports suggest that ET increases ATPS activity and S uptake in Brassica.²¹

Among the classical plant hormones connected to abiotic stress especially salinity and drought, ABA is the most important. In plants, oxidative stress induces SO₄²⁻ assimilation, as well as sulfite reductase, ATPS, APS reductase (APR), SAT, and SO₄²⁻ transporters.²² Furthermore, SO₄²⁻ affects ABA signaling to root-to-shoot and influence stomatal closure at the time of drought.²³ Another S containing gaseous molecule H₂S worked at the downstream pathway of ABA and upstream pathway of NO, which aid in ABA modulated stomatal closure to cope up with drought.²⁴ Thus, ABA is greatly interconnected with S assimilation rather than simple regulation.

There is a great interaction between SA mediated S assimilation and stress defense response. Plants receiving exogenous SA were found with elevated GSH content, along with higher GR activity,²⁵which confirms the interacting role among SA and S. Despite increasing GSH content, SA increases Cys and S content, ATPS and SAT activity,²⁶ while SA homeostasis is regulated by a sulfo-transferase (SOT12) via sulfation.²⁷ Glucosinolate accumulation in plant tissue is adversely affected by SA.²⁸ On the other hand, SA signaling is greatly controlled through S-nitrosylation, hence, require GSH for the activity. Therefore, further research is required for establishing the relation between SA and S metabolism.

The roles of GAs in regulating S assimilation enzymes are crucial for acquired abiotic stress tolerance in plants. Koprivova et al.¹⁸ reported that APR transcript levels induction by salinity could be prevented in gai mutant by disrupting GA signaling, but enzyme activity remains unchanged. A recent report suggested that GA and S together decrease oxidative stress by ethylene formation and promoting S use efficiency, photosynthesis and GSH production of Cd stressed plants.²⁹ For the regulation of S assimilation BRs can be modified by sulfation and sulfotransferases, thus exert their role on S metabolism.³⁰

The interplay of S with nitric oxide

Nitric oxide is reported to be involved in decreasing oxidative damage through GSH generation under various abiotic stresses.¹ In contrary, S supplementation increase GSH content in plant tissue by increased S assimilation.³¹ Thus, maybe there is an obvious interaction between S and NO. Nitric oxide also stimulates assimilation of S and react with targeted molecules thus decrease the ROS damage through the enhancement of antioxidant defense. Furthermore, NO interacts in the expression of some stress-responsive genes.³² For establishing the abiotic stress tolerance, NO avowedly or obliquely upregulates different genes connected with redox state of cells.³³ The relationship between the antioxidants and NO is mainly lighted upon GSH, which is enormously significant for controlling of ROS.³⁴ As a signaling molecule, NO activity controls S-utilization for GSH production under abiotic stress condition.³² The efficiency of AsA-GSH cycle and antioxidant defense mechanism mainly depends on the GSH content and redox homeostasis.¹ Thus NO is vital for stress tolerance in plants.

In the NO metabolic pathway, the reaction between NO or NO derived ONOO⁻ and GSH is vital to form an intermediate S-nitrosoglutathione (GSNO), which can further donate NO³⁵ (Figure 1). Under abiotic stress condition GSNOR take part in either limiting or alleviating NO levels in cells to tolerate stress.³⁶ The enzyme GSNOR, break down GSNO to release NO and form NH₃ and GSSG. Further GSSG is reduced to GSH by the activity of GR and balance redox homeostasis. Hence homeostasis of the enzyme GSNOR is imperative for stress tolerance in plants³⁷ and vital for regulating downstream ROS and RNS effects.³⁴

A further important interacting role of S exists with NO via H₂S – another important signaling molecule in plant physiology. Applying NaHS as an H₂S donor to Pb-stressed Sesamum indicum plants increased the NO content in root tissue, which hinted the H₂S induced NO signaling in Pb-stress tolerance.³⁸ Li et al.³⁹ also found that the H₂S–induced NO generation is essential for Cd tolerance in Medicago sativa. Similar results were also reported by Chen et al.⁴⁰ in barley seedling roots under salt stress and Li et al.⁴¹ under heat stress in Zea mays. Furthermore, exogenous SNP application enhanced the H₂S content, suggesting NO as an upstream signaling molecule for H₂S production in cells.³⁹ Shi et al.³⁸ observed that the NO-induced Cd tolerance in bermuda grass could be inhibited by both NO and H₂S scavengers, and stated that the NO responses were mediated via the H₂S signal. Therefore, it can be concluded that both NO and H₂S interaction offer plants tolerance to abiotic stress.

Polyamines and S interaction

Putrescine (Put), spermidine (Spd), and spermine (Spm) are the three major PAs originate in plants and are synthesized successively in the same biosynthetic pathway. S-Adenosyl methionine is one of the routs for PA biosynthesis. In this process SAM is decarboxylated with the action of SAM decarboxylase and the intermediate of this reaction is further act as the donor of aminopropyl sub-units for Spd and Spm biosynthesis⁸ (Figure 1). Here, Yang cycle functions to restore the S moiety in SAM and regulated by the S accessibility of the cell.⁴² Therefore, when plants suffer from S deficiency, PA biosynthesis is hampered, and as a result, the concentration of PA decreases.⁴³ Polyamines also take part in S assimilation as well as osmoprotection.¹⁷

Interaction with other plant nutrients

Sulfur interacts with all other essential plant nutrients, for instance, nitrogen, potassium (K), phosphorus, magnesium, molybdenum (Mo) and selenium. But among them, SO₄²⁻ supply alters K, Mo, and zinc (Zn), thus are strongly linked with the S availability. Researchers found a positive correlation between K and S content in shoots highlighted the interacting role of K⁺ as the counter cation of SO₄^2– during vacuolar storage and xylem loading in leaf tissue.⁴⁴ It is observed that Se treatment mimics S deficiency to activate specific SO₄²⁻ transporter expression to stimulate S uptake, resulting in the selenate-induced S accumulation in plants.⁴⁵

One of the important S-derivative – H₂S, has a profound effect on nutrient homeostasis thus conferring abiotic stress tolerance.⁴⁶ Although H₂S is produced in plants in a minor quantity, researchers have identified its nutrient balancing effects using NaHS as H₂S source exogenously. In a S-sufficient soil exogenous H₂S reduce S uptake by roots, but at S deficit condition, exogenous H₂S serves as S source for the normal metabolic process of plants.⁴⁴ Sulfur deficiency in plants triggers Mo and Zn uptake, but when S is supplied through H₂S fumigation, it prevents Mo and Zn uptake.⁴⁴ Exogenous NaHS enhanced absorption of P, S, Ca, Mg, and iron (Fe) in plants together with reduced the toxic Al accumulation. Moreover, exogenous NaHS increased the activity of H⁺-ATPase and Na⁺/K⁺-ATPase in Hordeum valgure.⁴⁷

In conclusion, S and their derivatives alone or interactively regulated many defense-related plant processes such as stomatal movement, redox balance, ion homeostasis and antioxidant defense. Glutathione, one of the key components of AsA-GSH cycle, is most important for antioxidant defense mechanism and controlling of ROS under abiotic stress condition. Nitric oxide signaling is largely dependent on S and GSH. On the other hand, S via H₂S can induce NO signaling in plants to increase abiotic stress tolerance. The interaction of S with PAs and some plant nutrients have been studied sporadically and therefore, warrants further investigation. This review briefly highlighted the recent progress on the interaction of S with other biomolecules to confer abiotic stress tolerance. However, further researches are necessary to elucidate the interacting role of S with ROS and other plant signals.

Conflicts of interest

There is no potential conflict of interest to disclose.