Cross-talk between sulfur assimilation and ethylene signaling in plants

Abstract

Sulfur (S) deficiency is prevailing all over the world and becoming an important issue for crop improvement through maximising its utilization efficiency by plants for sustainable agriculture. Its interaction with other regulatory molecules in plants is necessary to improve our understanding on its role under changing environment. Our knowledge on the influence of S on ethylene signaling is meagre although it is a constituent of cysteine (Cys) required for the synthesis of reduced glutathione (GSH) and S-adenosyl methionine (SAM), a precursor of ethylene biosynthesis. Thus, there may be an interaction between S assimilation, ethylene signaling and plant responses under optimal and stressful environmental conditions. The present review emphasizes that responses of plants to S involve ethylene action. This evaluation will provide an insight into the details of interactive role of S and ethylene signaling in regulating plant processes and prove profitable for developing sustainability under changing environmental conditions.

Introduction

Plant nutrition is a fundamental science that impacts all aspects of cropping systems, environmental sustainability, and human health and well being.¹ Sulfur (S) is a critical nutrient for metabolism, plant growth and development.^2,3 The importance of S as a plant nutrient has been recognized since long time but active research started in the second half of the 20th century when widespread S deficiencies were observed.⁴ Different crops have different demands for S, and the adequate supply of S increases crop yields appreciably.²

Sulfur plays an inevitable and imperative role in the formation of amino acids, methionine (Met; 21%) and cysteine (Cys; 27%), synthesis of protein, chlorophyll and oil in the oilseed crops.⁵ The process of S acquisition and assimilation play an integral role with plant metabolism, and its deficiency leads to reduced chlorophyll content, pigment system II (PS II) efficiency and ribulose 1,5-bisphosphate carboxylase (Rubisco) content.⁶ Excess sulfate transported into leaf cells accumulates mainly in the vacuoles and constitutes a large internal S reserve.⁷ Conversely, in some circumstances, S may be present in abundance, and regulatory mechanisms will favor a limitation of uptake and assimilation. The rationale is to avoid excess uptake, which is energetically wasteful and/or to avoid potential osmotic imbalances.⁸

A good part of S incorporated into organic molecules in plants is located in thiol (-SH) groups in proteins (Cys-residues) or non-protein thiols, (reduced gluthione; GSH).^9-12 These bonds are important for the stabilization of protein structure. The sensing of S nutrition state occurs through elaborate systems that modulate flux involving different component pathways.¹³ Cysteine is the donor of reduced S for the synthesis of Met and other S-containing metabolites.¹⁴ Methionine is the precursor for S-adenosyl methionine (SAM), the precursor for ethylene¹⁵ (Fig. 1), polyamines, and nicotinamine which is important for Fe nutrition in plants.^16,17

Figure 1. Schematic representation of regulatory interaction between sulfur assimilation and ethylene biosynthesis linked with ascorbate-glutathione pathway. ATPS, ATP sulfurylase; APR, adenosine 5-phosphosulfate reductase; SiR, sulfite reductase; ; OAS, O-acetylserine; OASTL, O-acetylserine (thiol) lyase; GR, glutathione reductase; GSH, glutathione reduced; GSSG, glutathione oxidized; SAM, S-adenosyl methionine; ACC 1-aminocyclopropane carboxylic acid; ACS, ACC synthase; ACO, ACC oxidase; GCL, Glutamate cysteine ligase; GSHS, GSH synthetase; ASC, ascorbate; DHA, dehydroascorbate; DHAR; DHA reductase; MDHA, monodehydroascorbate; MDHAR, MDHA reductase; APX, ascorbate peroxidase ; SOD, Superoxide dismutase.

Examples of regulation of plant development by S and phytohormones are provided under optimal and abiotic stress.^18-20 The present review discusses the interrelation between S assimilation, ethylene action and plant functions. This evaluation will provide an insight into the mechanisms in plants on S assimilation and ethylene signaling that can be successfully exploited in developing plant vigour under optimal and stressful environmental conditions.

Regulation of Sulfur Assimilation

Sulfate assimilation is highly regulated in a demand-driven manner.^19,21,22 The pathway is induced when there is a high demand for growth and development.²³ A surplus of reduced S compounds represses the pathway.¹⁴ It has been reported in barley that the uptake capacity reached a maximum after 4 d of S deprivation and even decreased after this; however, sulfate transporter mRNA abundance continued to increase.²⁴ In a similar experiment with potato, the sulfate transporter mRNA abundance increased over an 8 d period; however, the measured increased uptake capacity showed only a transient rise.²⁵ It was proposed that a repression mechanism operated in which some downstream reduced S compounds acted to repress uptake, probably acting on the transcription of the genes for the uptake transporters.²⁶ When S supply becomes limiting, the levels of these compounds fall and the repression is relieved. Indirect evidence using inhibitors supported a rapid turnover of the sulfate transporter proteins and the importance of transcriptional regulation.^26,27

Sulfate withdrawal from the growing medium decreases the levels of sulfate, Cys and GSH in plant tissues leading to the induction of sulfate transporter systems and key enzymes along the assimilatory pathway.^21,28 The increase in steady-state levels of mRNAs for high-affinity sulfate transporters, ATP-sulfurylase (ATPS), and adenosine 5-phosphosulfate reductase (APR) upon S starvation has been detected by Northern analysis^29,30 or cDNA arrays.^31,32 It reveals that the de-repression is regulated at the level of transcription. This de-repression correlates with the time of exposure to S-deficiency; and the activity of APR and ATPS quickly returns to the normal levels when plants are supplied with sulfate again.^21,33 O-acetylserine accumulates during S starvation and may thus serve as a signal of the S status.³⁴ O-acetylserine acts most probably as a transcriptional regulator since its addition strongly increases mRNA levels of all the three APR isoforms and also those of sulfite reductase (SiR), chloroplastic O-acetyl serine (thiol) lyase (OAS-TL), and cytosolic serine acetyl transferase (SAT).³⁵ O-acetylserine plays a regulatory role in the synthesis of Cys by controlling the oligomerization of the Cys synthase complex, thus coordinating between serine as the nitrogen (N) source and sulfide as the sulfate assimilation intermediate.³⁶

An Overview of Ethylene Biosynthesis

Ethylene (C₂H₄) is a simple gaseous plant hormone that has profound effects upon plant growth and development. It regulates diverse aspects of plant growth and development, including germination; leaf, stem, and root growth; sex determination; fruit ripening; organ abscission; leaf and flower senescence; and cell death of the cereal endosperm.^37,38 Ethylene before being recognized as a plant hormone played a role in the history of agriculture. The historical techniques to promote fruit ripening are ancient Egyptians cutting sycamore figs and the Chinese burning incense to ripen pears,^39,40 all of these practices released ethylene gas, which promoted fruit ripening. It was in 1795 that ethylene was combined with chlorine gas to produce oil of the Dutch chemists. For its part in the process, ethylene was known as olefiant gas – or oil-making gas,⁴¹ and it became a compound of commercial interest. Later, with the introduction of a standard nomenclature system, olefiant gas was named ethylene. The chronology of events has been conveyed in great detail in the works of Abeles et al.³⁸ and Chaves and de Mello-Farias.⁴⁰

The biosynthesis of ethylene occurs through a relatively simple metabolic pathway that has been extensively studied and well documented in plants.^42-44 Ethylene is derived from the amino acid Met. Methionine is converted to SAM by the enzyme SAM synthetase. S-adenosyl methionine is then converted by 1-aminocyclopropane carboxylic acid (ACC) synthase (ACS) to ACC and 5´-deoxy-5´-methylthioadenosine (MTA). Conversion of SAM into ACC is the rate-limiting step in the pathway. ACC oxidase (ACO) catalyzes the conversion of ACC to ethylene. Thus, these two (ACS and ACO) are the important enzymes that are involved in the formation and oxidation of the immediate precursor of ethylene i.e., ACC (Fig. 1). The final conversion of ACC to ethylene is oxygen dependent⁴³ and yields CO₂ and cyanide as by-products. ACC oxidase may play an important role in regulating ethylene biosynthesis, especially during conditions of high ethylene production.

Besides formation of ACC and subsequently its conversion to ethylene, ACS is also involved in catalyzing the conversion of SAM into MTA. These enzymatic reactions appear to be the rate-limiting step in the formation of ethylene but there are situations where ACO is absent and ACS and ACO are induced, for example by wounding and the ripening stimulus.⁴⁵ The conversion of ACC to ethylene catalyzed by ACO is oxygen dependent, and, under anaerobic conditions, ethylene formation is completely suppressed. In this reaction, Fe²⁺ and ascorbic acid (AsA) are required as a cofactor and a co-substrate, respectively. The other reaction product, MTA, must be recycled back into the Met pathway to provide an adequate supply of Met as substrate for the continual production of ethylene. The poisonous gas hydrogen cyanide formed from the decomposition of ACC to ethylene is detoxi□ed by β-cyanoalanine synthase. Different expression of ACS and ACO isozymes encoded by multigene families in response to external and internal stimuli is controlled at the transcriptional and post transcriptional level.^46,47

In plants, ethylene biosynthesis is controlled by two systems: the ethylene autoinhibitory system 1, which generally operates during normal vegetative growth of plant; and system 2, regulated by a positive feedback mechanism, usually responsible for the rapid increase in ethylene production in senescing ethylene-sensitive plant organs, and in ripening climacteric fruits.⁴⁸ In Arabidopsis, the N-terminal fragments of five ethylene receptors (subfamily 1, ETR1 and ERS1; subfamily 2, ETR2, ERS2, and EIN4) are involved in copper-mediated ethylene binding.

Plants under biotic or abiotic stress, such as pathogen attack, salt, wounding, drought, heat, flooding, low phosphorus,⁴⁹ and low iron⁵⁰ produce higher levels of ethylene than non-stressed plants. It is now becoming clear that various ethylene-regulated stress responses are essential for stress tolerance and the survival of plants. For example, the submergence tolerance in rice (Oryza sativa) is determined by the levels of ethylene and the activity of SUBMERGENCE1A (SUB1A), which is induced by ethylene.^51-53 In addition, ethylene-insensitive mutants (etr1–1, ein2–1, and ein4–1) are more sensitive to high salt concentrations than the wild type, whereas a constitutive ethylene response mutant (ctr1–1) is more tolerant, supporting the important role of ethylene in salt stress signaling.^54,55 Ethylene production increases when plants are deprived of potassium (K),⁵⁶ and ethylene-insensitive mutants are more sensitive to low K⁺ in terms of leaf chlorosis and shoot growth than is the wild type. These findings show ethylene as an important component in the plant response to low K⁺ stress.

Plants exposed to environmental stresses speed up their rate of ethylene production. Various types of stress induce enhanced production of ethylene from plant tissues.³⁸ However, the mechanism of ethylene biosynthesis is same under stress as under optimal environmental conditions. Stress induces the synthesis of stress ethylene because of the burst of ethylene that occurs under stress. When plants are exposed to conditions that threaten their ability to survive, the same mechanism that produces ethylene for normal development instead functions to produce what is known as stress ethylene.⁵⁷ The functions of normal and stress ethylene differ considerably although both are produced by the same pathway.

Responses to Sulfur Involve Phytohormones Action

Sulfur availability affects phytohormone action and S assimilation may interact with phytohormones. Koprivova and Rennenberg²³ reported that phytohormones play important role in reduced GSH synthesis. cDNA arrays revealed the induction of genes involved in auxin synthesis upon S-starvation, pointing to a possible role of phytohormones under S deficiency.^23, Ohkama et al.³⁴ used transgenic Arabidopsis plants, expressing β_SR-driven green fluorescent protein (GFP) under the control of a chimeric promoter containing the sulfur-responsive element of β-conglycinin³⁸ to test the influence of phytohormones on the sulfur-deficiency response. Whereas abscisic acid (ABA), indole-3-acetic acid (IAA), ACC (precursor of ethylene), gibberellic acid (GA), and jasmonic acid (JA) were not able to induce the expression of GFP derived from the sulfur-responsive element and, thus, mimic the sulfur-starvation response, trans-zeatin caused an increase in GFP synthesis both in sulfur-sufficient and sulfur-deficient conditions. In addition, zeatin treatment resulted in an increased accumulation of mRNA for APR and a low-affinity sulfate transporter.³⁴

Thus, it is not surprising to see increasing evidence of coordination between nutritional and hormonal signaling.⁵⁹ Schachtman and Shin⁶⁰ reported that the plant hormones cytokinin, IAA, and JA were signaling components in response to S deficiency. The expression of APR1 is upregulated by S deficiency⁶¹ and also by exogenous cytokinin.³⁴ Exogenous cytokinin downregulates the expression of the high-af□nity transporter SULTR;2⁶², which is upregulated by S deprivation. Cytokinin acts through the cytokinin response receptor (CRE1) to regulate sulfate uptake and transporter expression. In the cre1–1 mutant, application of cytokinin only partly reduces sulfate uptake, suggesting redundancy as noted for the case of phosphate deprivation.⁶³

Auxin is also a signaling component under sulfate limitation.³² The expression of auxin-inducible genes (IAA18, At1g51950, tryptophan synthase β chain, At5g38530, putative auxin-regulated protein, At2g33830) is upregulated by S starvation.^32,64 The expression of NIT3 nitrilase, which can convert indole-3-acetonitrile to IAA, is strongly increased by S starvation.⁶⁵ The increased auxin production may result in an increase in lateral root density in Arabidopsis under sulfate-limited conditions.⁶⁶

Jasmonic acid is also a possible signaling component in leaves. Genes involved in JA biosynthesis are upregulated under S deficiency.^67,68 These genes include 12-oxophytodienoate reductase 1 and lipoxygenase.^31,32,67 Jasmonic acid may regulate the expression of genes involved in sulfate assimilation and GSH synthesis.^68,69 Furthermore, methyl jasmonate is involved in regulating the activity of S assimilation enzymes such as SAT and APR.⁶⁹ Although JA is a regulator of S metabolism, its levels in plants are not well characterized under deficient conditions. Recently, an ethylene insensitive like (EIL) transcription factor, SLIM1, was isolated and shown to be involved in the regulation of a high-affinity sulfate transporter in response to sulfate limitation.⁷⁰

The other level of interaction of nutrient and hormone may be visualized at the level of reactive oxygen species (ROS) production. ROS have important consequences that lead to aerenchyma formation in nutrient-deprived roots,⁷¹ which may be an important adaptation that lowers the cost of maintaining roots.⁷² Direct evidence showing that ROS is a signaling component in S-starved plants is not yet available. However, in Bacillus subtilis several genes involved in S-assimilation and synthesis of S-containing amino acids were induced by adding paraquat.⁷³ The amount of ROS visualized after 30 h of S deprivation in roots was greater than in sulfate-sufficient roots.⁶⁰ The regulation and interaction between ROS and ascorbate-glutathione (AsA-GSH) cycle impacts the synthesis of plant hormones such as SA, GA, ABA, and ethylene,^74,75 which may signal plant response to nutrients deficiency. The involvement of ROS in S signaling may be more complex than that of K deprivation because the AsA-GSH cycle, i.e., downstream of sulfate assimilation is involved in the removal of H₂O₂.

Ethylene Cross-Talk Associated with Sulfur

The interaction between ethylene and S has been shown to control the regulation of plants processes and abiotic stress tolerance. The first organic compound synthesized in the sulfate assimilatory pathway is Cys. Cysteine is the final product of S-assimilation. It is the precursor and S donor for the majority of other organic S compounds present in plants^14,76 such as Met, SAM, S-methyl methionine, [Fe/S] clusters, hormones, vitamins and enzyme cofactors.⁷⁶ The main pathway for ethylene biosynthesis comes from Met. Methionine is a fundamental metabolite in plant cells because it controls the level of several key metabolites, such as ethylene, polyamines and biotin through its first metabolite, SAM. It is first converted to SAM, then ACC, and finally ethylene in three consecutive reactions catalyzed by the enzymes of SAM synthetase, ACS and ACO, respectively⁷⁷ (Fig. 1).

Further, Bürstenbinder et al.¹⁵ using an mtk mutant, that has a disruption of the Yang cycle, reported that the Yang cycle contributes to SAM homeostasis, especially when de novo SAM synthesis is limited, such as at S starvation.⁷⁸ They also showed that this cycle was required to sustain a high level of ethylene synthesis. However, additional evidence suggests that in addition to recycling the Met moieties via the Yang cycle, the de novo synthesis of Met is required when high rates of ethylene production are induced.⁷⁹

Moreover, S availability and ethylene have been shown to regulate GSH synthesis and stress tolerance to ozone⁸⁰ and Cd^81,82 stress. Glutathione acts as a storage and transport form for Cys; otherwise the excess Cys present in the cell becomes toxic.^83-86 Glutathione acts as a signal, controlling the inter-organ regulation of S nutrition and is mainly confined to the leaves.^87,88 During S deficiency GSH content rapidly decreased in tobacco cell cultures but was rebuilt upon the re-supply of sulfate and/or Cys.⁸⁹ Glutathione is reduced in plants subjected to S deficiency.³² The reduced form of glutathione, GSH, is an abundant compound in plant tissue that exists interchangeably with the oxidized form, GSSG. GSH is abundant (3–10 mM) in cytoplasm, nuclei and mitochondria and is the major soluble antioxidant in these cell compartments. Glutathione has been associated with several growth and development related events in plants, including cell differentiation, cell death and senescence, pathogen resistance and enzymatic regulation⁸⁶ and its content is affected by S nutrition.^90,91 Glutathione is the major reservoir of non-protein S. It is the major redox buffer in most aerobic cells, and plays an important role in physiological functions, including redox regulation, conjugation of metabolites, detoxification of xenobiotics and homeostasis and cellular signaling that triggers adaptive responses.⁸⁶ It also plays an indirect role in protecting membranes by maintaining α-tocopherol and zeaxanthin in the reduced state. It can also function directly as a free radical scavenger by reacting with superoxide, singlet oxygen and hydroxyl radicals. Glutathione protects proteins against denaturation caused by the oxidation of protein thiol groups under stress. The central role of GSH in the antioxidative defense system is due to its ability to regenerate another water soluble antioxidant, AsA, in ascorbate-glutathione (AsA-GSH) cycle.⁸⁶ The increased demand for GSH can be met by the activation of pathways involved in S assimilation and Cys biosynthesis. Its concentration is controlled by a complex homeostatic mechanism where the availability of S seems to be required.⁹² Manipulation of GSH biosynthesis increases resistance to oxidative stress.^19,20

Glutathione reductase (GR) is a flavo-protein oxidoreductase, found in both prokaryotes and eukaryotes⁸⁶ and maintains the balance between GSH and AsA pools, which in turn maintain cellular redox state. The enzyme protein, although synthesized in the cytoplasm, can be targeted to both chloroplast and mitochondria.⁹³ In higher plants, GR is involved in defense against oxidative stress, whereas, GSH plays an important role within the cell system, which includes participation in the AsA-GSH cycle, maintenance of the -SH group and a substrate for glutathione-S-transferases.⁹⁴ Glutathione reductase and GSH play a crucial role in determining the tolerance of a plant during environmental stresses.⁹⁵ In almost all the biological functions, GSH is oxidized to oxidised glutathione (GSSG) which should be converted back to GSH in plant cell to perform normal physiological functions. Supplementary S fertilization to high S loving crops such as brassicas and leguminous crops has been shown to enhance plant-stress-defense operations and act indirectly by improving general plant performance under abiotic and biotic stresses as well through improving GSH and AsA.^12,96

There are reports that demonstrate a functional link between ethylene and S. Ethylene plays important roles in selenite resistance in Arabidopsis.⁹⁷ A comprehensive gene expression analysis showed that transcripts regulating ethylene synthesis (ACS6) and signaling (ERF) were upregulated by selenate treatment, and plants overexpressing ERF1 exhibited an increase in selenium (Se) resistance.⁹⁸ These results indicate that Se resistance achieved through ethylene signaling is not mediated by S starvation resulting from the Se treatment but is a Se-specific response. The resistance mechanism may involve ethylene-enhanced S uptake and assimilation, as observed in Arabidopsis thaliana accessions, Columbia (Col)-0. The higher levels of organic S compounds observed in Col-0 may enable it to more efficiently prevent Se analogs from replacing S in proteins and other S compounds,⁹⁷ but no direct study is available regarding ethylene and S. However, the role of ethylene in various nutrients deficiency is available.^49,99-107 Reports on the interaction of S and ethylene are still in its infancy. Koprivova et al.¹⁰⁸reported that the application of 0.2 mM ACC, which stimulates ethylene production increased accumulation of APR activity. Recently, it has been shown that ethylene action in mustard is dependent on S availability.^81,82 Disruption of JA and ethylene signaling pathway prevented GSH accumulation under salt stress. There is an indication that APR activity is increased in salt stress if ethylene signaling is disturbed, but GSH will not accumulate suggesting that components of GSH biosynthesis are under the control of ethylene¹⁰⁸ (Fig. 1). Selenate induces S starvation and activates genes controlling S assimilation.¹⁰⁹ A Se-induced S starvation response is further suggested by the 30-fold upregulation of a thioglucosidase (At3g60140), thought to break down glucosinolates; these compounds are S-containing secondary metabolites and their catabolism may recycle a limited pool of S.^31,110 Microarray analysis also suggests that Se treatment induces the synthesis of ethylene.⁹⁸ Thus Se reduces S assimilation and induces ethylene synthesis.

In plants exposed to various types of abiotic and biotic stresses, increased ethylene levels correspond to increased damage, implying that stress ethylene is deleterious to plants. However, it was also reported that transcriptional activation of ERF in ethylene signaling process enhances stress tolerance in tobacco seedlings by decreasing ROS accumulation in response to salt, drought and freezing.¹¹¹ It may be that these discrepancies are due to differences in the amount of endogenous ethylene production, and in the period of stress treatment, in addition to the plant tissue studied.¹¹² Studies have shown that MPK3/6 can be activated by many stress signals in minutes, which are also able to trigger ethylene production in hours.^113-115 Yoshida et al.⁸⁰ studied the defensive roles of ethylene and SA against ozone. Macroarray analysis suggested that the ethylene and SA defects influenced GSH metabolism and they protected against ozone-induced leaf injury by increasing de novo biosynthesis of glutathione. Elevated oxidative stresses caused by environmental stimuli, including ozone, UV-B, and wounding have been demonstrated to enhance ethylene production via ACS and ACO.¹¹⁶ In ozone treatment, ethylene also enhanced ROS generation, which in turn leads to cell death.¹¹⁶ In sweet potato, a wound-inducible ipomoelin (IPO) gene expression can be induced by ethylene,¹¹⁷ but was completely repressed by diphenylene iodonium, an inhibitor of NADPH oxidase.¹¹⁸ These studies suggest that elevated oxidative stress may play important role in ethylene biosynthesis, ethylene signaling, and ethylene-mediated effects. Several studies suggest that shoot elongation in submerged plants may be controlled by phytohormones, and in particular by ethylene production, as in flood-tolerant Rumex species.^119,120 Zhang and Huang¹²¹ reported that treatment of ethylene biosynthesis inhibitor or ethylene receptor antagonist, i.e., blockage of ethylene biosynthesis or the ethylene signaling pathway decreases freezing tolerance of overexpressing TERF2/LeERF2 tobaccos. In addition, gene profiling studies also showed that ethylene might be involved in cold response.¹²² Zhang et al.¹²³ reported that ERF proteins regulate a variety of stress responses in plant. JERF1, a tomato ERF protein, can be induced by ABA. Overexpression of JERF1 enhanced the tolerance of transgenic tobacco to high salt concentration, osmotic stress, and low temperature by regulating the expression of stress-responsive genes by binding to DRE/CRT and GCC-box cis-elements. The internodes elongation response, which serves as an important adaptation response in deepwater rice, is also controlled by ethylene.¹²⁴ Ethylene responsive factors (ERFs) play an important role in plant responses to stresses. SlERF1 played a positive role in the salt tolerance of tomato plants.¹²⁵ Considering the cross-talk between S and ethylene signaling, the performance of plants could be achieved under optimal and changing environment.

Conclusion

Sulfur is an important macronutrient crucial for plant growth and vigour, and crop yield, and resistance to stressful environments. Plants assimilate sulfate and reduce to cysteine and methionine, which constitute about 80–90% of total sulfur in most plants. Cysteine is an important link for the formation of non-protein thiol, GSH, a major plant constituent of storage S, and ethylene through the formation of SAM. Under optimal environmental conditions, S and ethylene regulate physiological processes interdependently, while conditions of stressful environments lead to enhanced S assimilation capacity and GSH synthesis. Under these conditions, ethylene signaling also regulates GSH synthesis for better adaptation of plants. Thus, an interaction exists between S and ethylene to control plant development under optimal and stressful environments. Although our scientific understanding of the molecular mechanisms of ethylene biosynthesis, perception and signaling has been improved considerably, but there are still major challenges concerning interaction or cross-talk between ethylene and S in crop plants under various environmental conditions.

Ethylene is a pivotal signaling molecule, and while its connection to all plant processes is yet not completely understood, a picture is emerging of a simple molecule whose concentration can be manipulated to create many desirable traits in plants. Study of the ethylene biosynthesis pathway in plants made it possible to modify and insert genes that alter the level of ethylene produced in response to various stimuli. Enzymes that degrade SAM or ACC, the precursors of ethylene, have been shown to effectively reduce ethylene levels without drastically altering the physiology of the plant. Expression of sense or antisense versions of enzymes from the ethylene biosynthesis pathway should also allow for genetic control of ethylene levels. It is also crucial to address how ethylene signaling and changes in gene expression are integrated into specific agronomic traits. A detailed understanding of molecular and cellular details in crop plants on ethylene signaling and S assimilation under different environmental conditions will provide innovative tools for sustainable plant development.

Glossary

Abbreviations:

S

sulfur

Cys

cysteine

GSH

reduced glutathione

SAM

S-adenosyl methionine

Met

methionine

Rubisco

ribulose 1,5-bisphosphate carboxylase

ATPS

ATP-sulfurylase

APR

adenosine 5-phosphosulfate reductase

SiR

sulfite reductase

OAS-TL

O-acetyl serine (thiol) lyas

ACS

1-aminocyclopropane carboxylic acid synthase

ACO

ACC oxidase

ABA

abscisic acid

IAA

indole-3-acetic acid

GA

gibberellic acid

JA

jasmonic acid

SAT

serine acetyl transferase

GR

glutathione reductase

GSSG

oxidized glutathione

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.