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Sulfur assimilation is the process by which living organisms incorporatesulfur into their biological molecules.[1] In plants, sulfate is absorbed by the roots and then transported to the chloroplasts by the transpiration stream where the sulfur are reduced tosulfide with the help of a series ofenzymatic reactions. Furthermore, the reduced sulfur is incorporated intocysteine,[2] an amino acid that is a precursor to many other sulfur-containing compounds. In animals, sulfur assimilation occurs primarily through the diet, as animals cannot produce sulfur-containing compounds directly. Sulfur is incorporated into amino acids such ascysteine andmethionine, which are used to buildproteins and other important molecules.[2]
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Sulfate uptake occurs in roots.[3] The maximal sulfate uptake rate is generally already reached at sulfate levels of 0.1 mM and lower. The uptake of sulfate by the roots and its transport to the shoot appears to be one of the primary regulatory sites of sulfur assimilation.[3]
Sulfate is actively taken up across theplasma membrane of theroot cells, subsequently loaded into thexylem vessels and transported to the shoot by thetranspiration stream.[4] The uptake and transport of sulfate is ATP-dependent.[5] Sulfate is reduced in the chloroplasts. Sulfate in plant tissue is predominantly present in thevacuole, since the concentration of sulfate in thecytoplasm is kept rather constant.
Distinct sulfate transporter proteins mediate the uptake, transport and subcellular distribution of sulfate.[6] The sulfatetransportersgene family has been classified in up to 5 different groups according to their cellular and sub-cellulargene expression, and possible functioning.[7] Each group of transporter proteins may be expressed exclusively in the roots or shoots of the plant, or both.
Regulation and expression of the majority of sulfate transporters are controlled by the sulfurnutritional status of the plants.[8] Upon sulfate deprivation, the rapid decrease in root sulfate is regularly accompanied by a strongly enhanced expression of most sulfate transporter genes (up to 100-fold) accompanied by enhanced sulfate uptake capacity. It is not yet fully understood whether sulfate and other metabolic products of sulfur assimilation (O-acetylserine,cysteine,glutathione) act as signals in the regulation of sulfate uptake and transport, or in the expression of the sulfate transporters involved.
Sulfate reduction predominantly takes place in the leafchloroplasts. Here, the reduction ofsulfate tosulfide occurs in three steps beginning with its conversion toadenosine 5'-phosphosulfate (APS). This first step is catalyzed byATP sulfurylase. The affinity of this enzyme for sulfate is low (Km approximately 1 mM), and the in situ sulfate concentration in the chloroplast is most likely one of the limiting/regulatory steps in sulfur reduction. Subsequently, APS is reduced to sulfite, catalyzed by APS reductase.Glutathione is the propsedreductant.
The latter reaction is assumed to be one of the primary regulation points in the sulfate reduction, since the activity of APS reductase is the lowest of the enzymes of the sulfate reduction pathway and it has a fast turnover rate.Sulfite is with high affinity reduced bysulfite reductase tosulfide withferredoxin as a reductant. The remaining sulfate in plant tissue is transferred into thevacuole. The remobilization and redistribution of the vacuolar sulfate reserves appear to be rather slow and sulfur-deficient plants may still contain detectable levels of sulfate.[9]
Sulfide is incorporated intocysteine, catalyzed by O-acetylserine (thiol)lyase, with O-acetylserine as substrate. The synthesis of O-acetylserine is catalyzed byserine acetyltransferase and together with O-acetylserine (thiol)lyase it is associated as enzyme complex namedcysteine synthase.
The formation of cysteine is the direct coupling step between sulfur (sulfur metabolism) andnitrogen assimilation in plants. This differs from the process in yeast, where sulfide must be incorporated first inhomocysteine then converted in two steps to cysteine.
Cysteine is sulfur donor for the synthesis ofmethionine, the major other sulfur-containing amino acid present in plants. This happens through thetranssulfuration pathway and the methylation ofhomocysteine.
Both cysteine and methionine are sulfur-containingamino acids and are of great significance in the structure, conformation and function ofproteins andenzymes, but high levels of these amino acids may also be present in seed storage proteins. The thiol groups of the cysteine residues in proteins can be oxidized resulting indisulfide bridges with other cysteineside chains (and formcystine) and/or linkage ofpolypeptides.
Disulfide bridges (disulfide bonds) make an important contribution to the structure of proteins. Thethiol groups are also of great importance in substrate binding of enzymes, in metal-sulfur clusters in proteins (e.g.ferredoxins) and in regulatory proteins (e.g.thioredoxins).
Glutathione or its homologues, e.g. homoglutathione inFabaceae; hydroxymethylglutathione inPoaceae are the major water-soluble non-proteinthiol compounds present in plant tissue and account for 1-2% of the total sulfur.[10] The content of glutathione in plant tissue ranges from 0.1 – 3 mM. Cysteine is the direct precursor for the synthesis of glutathione (and its homologues). First, γ-glutamylcysteine is synthesized from cysteine and glutamate catalyzed bygamma-glutamylcysteine synthetase. Second, glutathione is synthesized from γ-glutamylcysteine andglycine (in glutathione homologues,β-alanine orserine) catalyzed by glutathione synthetase. Both steps of the synthesis of glutathione are ATP dependent reactions.[11] Glutathione is maintained in the reduced form by anNADPH-dependentglutathione reductase and the ratio of reduced glutathione (GSH) tooxidized glutathione (GSSG) generally exceeds a value of 7.[12]Glutathione fulfils various roles in plant functioning. In sulfur metabolism it functions as reductant in the reduction of APS to sulfite. It is also the major transport form of reduced sulfur in plants. Roots likely largely depend for their reduced sulfur supply on shoot/root transfer of glutathione via thephloem, since the reduction of sulfur occurs predominantly in the chloroplast. Glutathione is directly involved in the reduction and assimilation ofselenite intoselenocysteine. Furthermore, glutathione is of great significance in the protection of plants against oxidative and environmental stress and it depresses/scavenges the formation of toxicreactive oxygen species, e.g.superoxide,hydrogen peroxide and lipidhydroperoxides. Glutathione functions as reductant in the enzymatic detoxification of reactive oxygen species in the glutathione-ascorbate cycle and as thiol buffer in the protection of proteins via direct reaction with reactive oxygen species or by the formation of mixed disulfides. The potential of glutathione as protectant is related to the pool size of glutathione, its redox state (GSH/GSSG ratio) and the activity ofglutathione reductase. Glutathione is the precursor for the synthesis of phytochelatins, which are synthesized enzymatically by a constitutive phytochelatin synthase. The number of γ-glutamyl-cysteine residues in the phytochelatins may range from 2 – 5, sometimes up to 11. Despite the fact that thephytochelatins form complexes which a few heavy metals, viz.cadmium, it is assumed that these compounds play a role in heavy metalhomeostasis and detoxification by buffering of the cytoplasmatic concentration of essential heavy metals. Glutathione is also involved in the detoxification ofxenobiotics, compounds without direct nutritional value or significance in metabolism, which at too high levels may negatively affect plant functioning. Xenobiotics may be detoxified in conjugation reactions with glutathione catalyzed byglutathione S-transferase, which activity is constitutive; different xenobiotics may induce distinctisoforms of the enzyme. Glutathione S-transferases have great significance inherbicide detoxification and tolerance in agriculture and their induction by herbicideantidotes ('safeners') is the decisive step for the induction of herbicide tolerance in many crop plants. Under natural conditions glutathione S-transferases are assumed to have significance in the detoxification of lipidhydroperoxides, in the conjugation of endogenous metabolites,hormones andDNA degradation products, and in the transport offlavonoids.
Sulfolipids are sulfur containing lipids.Sulfoquinovosyl diacylglycerols are the predominant sulfolipids present in plants. In leaves its content comprises up to 3 - 6% of the total sulfur present.[13] This sulfolipid is present inplastidmembranes and likely is involved inchloroplast functioning. The route ofbiosynthesis and physiological function of sulfoquinovosyldiacylglycerol is still under investigation. From recent studies it is evident thatsulfite it the likely sulfurprecursor for the formation of thesulfoquinovose group of this lipid.
Brassica species containglucosinolates, which are sulfur-containingsecondary compounds. Glucosinolates are composed of a β-thioglucose moiety, a sulfonated oxime and a side chain. The synthesis of glucosinolates starts with the oxidation of the parent amino acid to analdoxime, followed by the addition of a thiol group (through conjugation with glutathione) to producethiohydroximate. The transfer of aglucose and a sulfate moiety completes the formation of the glucosinolates.
The physiological significance of glucosinolates is still ambiguous, though they are considered to function as sink compounds in situations of sulfur excess. Upon tissue disruption glucosinolates are enzymatically degraded bymyrosinase and may yield a variety of biologically active products such asisothiocyanates,thiocyanates,nitriles and oxazolidine-2-thiones. The glucosinolate-myrosinase system is assumed to play a role in plant-herbivore and plant-pathogen interactions.
Furthermore, glucosinolates are responsible for the flavor properties ofBrassicaceae and recently have received attention in view of their potential anti-carcinogenic properties.Allium species contain γ-glutamylpeptides andalliins (S-alk(en)yl cysteine sulfoxides). The content of these sulfur-containingsecondary compounds strongly depends on stage of development of the plant, temperature, water availability and the level of nitrogen and sulfur nutrition. In onionbulbs their content may account for up to 80% of the organic sulfur fraction.[14] Less is known about the content of secondary sulfur compounds in the seedling stage of the plant.
It is assumed that alliins are predominantly synthesized in the leaves, from where they are subsequently transferred to the attached bulb scale. The biosynthetic pathways of synthesis of γ-glutamylpeptides and alliins are still ambiguous. γ-Glutamylpeptides can be formed from cysteine (via γ-glutamylcysteine or glutathione) and can be metabolized into the corresponding alliins via oxidation and subsequent hydrolyzation by γ-glutamyltranspeptidases.
However, other possible routes of the synthesis of γ-glutamylpeptides and alliins may not be excluded. Alliins and γ-glutamylpeptides are known to have therapeutic utility and might have potential value as phytopharmaceutics. The alliins and their breakdown products (e.g.allicin) are the flavor precursors for the odor and taste of species. Flavor is only released when plant cells are disrupted and the enzyme alliinase from the vacuole is able to degrade the alliins, yielding a wide variety of volatile and non-volatile sulfur-containing compounds. The physiological function of γ-glutamylpeptides and alliins is rather unclear.
Unlike in plants, animals do not have a pathway for the direct assimilation of inorganic sulfate into organic compounds. In animals, the primary source of sulfur is dietarymethionine, an essential amino acid that contains a sulfur atom. Methionine is first converted toS-adenosylmethionine (SAM), a compound that is involved in many important biological processes, including DNAmethylation andneurotransmitter synthesis.
SAM can then be used to synthesize other important sulfur-containing compounds such ascysteine,taurine, andglutathione. Cysteine is a precursor for the synthesis of several important proteins and peptides, as well as glutathione, a powerful antioxidant that protects cells fromoxidative stress.Taurine is involved in a variety of physiological processes, includingosmoregulation,modulation ofcalcium signaling, and regulation of mitochondrial function.
Inbacteria andfungi, the sulfur assimilation pathway is similar to that in plants, where inorganic sulfate is reduced to sulfide, and then incorporated into cysteine and other sulfur-containing compounds.
Bacteria and fungi can absorb inorganic sulfate from the environment through a sulfate transporter, which is regulated by the presence of sulfate in the medium. Once inside the cell, sulfate is activated byATP sulfurylase to formadenosine 5'-phosphosulfate (APS), which is then reduced to sulfite by APS reductase. Sulfite is further reduced to sulfide by sulfite reductase, which is then incorporated into cysteine by enzyme.
Cysteine, once synthesized, can be used for the biosynthesis ofmethionine and other important biomolecules. In addition, microorganisms also use sulfur-containing compounds for various other purposes, such as the synthesis ofantibiotics.
Sulfur assimilation in microorganisms is regulated by a variety of environmental factors, including the availability of sulfur in the medium and the presence of other nutrients. The activity of key enzymes in the sulfur assimilation pathway is also regulated by feedback inhibition from downstream products, similar to the regulation seen in plants.
Sulfur assimilation is highly regulated and influenced by both external environmental factors and internal metabolic feedback pathways, in order to maintain sulfur homeostasis. Under sulfur-deficient conditions, plants modify their internal pathways to enhance sulfur uptake. In plants, a key regulator is thetranscription factor SLIM1 (Sulfur Limitation 1), which functions in activating genes involved in sulfur transport like SULTR1;2 (a high-affinity transporter) and those involved in sulfur assimilation like ATP sulfurylase and APS reductase.[15] The post-transcriptional regulation of these genes are done via amicroRNA called miR395. When sulfur uptake is sufficient and is no longer limited, this microRNA targets the SULTR2;1(a low-affinity transporter) and degrades/inhibits its translation.[16] Besides the transcriptional regulation of sulfur assimilation, there also lies post-translational mechanisms that control this process. This includes feedback inhibition by the accumulation of end products such asglutathione andcysteine, as well as regulation of the enzyme APS reductase which is activated or inhibited by theredox state of the cell.[17]
In fungi, specifically theAspergillus fumigatus, sulfur assimilation is managed by the transcription factor MetR.[18] This transcription factor functions similarly to SLIM1, in which under sulfur-limiting conditions it activates genes responsible for sulfur uptake.[19] MetR also plays a key role in protecting the fungus's virulence against the host-immune system.[18] Additionally, the regulation of sulfur plays an interconnected role with other nutrient cycles like carbon, nitrogen, and iron. For example, if MetR is impaired, the management of iron homeostasis is at risk. In plants, under sulfur-limiting conditions they optimize nitrogen assimilation to maintain metabolic homeostasis.[20]
In animals, since sulfur uptake is primarily obtained through the diet in the form of cysteine or methionine, the regulation of sulfur metabolism is done via thetranssulfuration pathway.[21] In this pathway, methionine is converted to homocysteine and then later converted to cysteine via the enzymesCystathionine Beta-synthase (CBS) andCystathionine gamma-lyase (CGL).[21] Cysteine is utilized for glutathione production, and high levels of glutathione feedback negatively to downregulate the enzymes CBS and CGL.[22]
Regulation of sulfur assimilation is tightly controlled to ensure balanced production of sulfur-compounds like cysteine, methionine, and glutathione.[17] These are key molecules that play a role in redox balance, and protein synthesis. Sulfur levels are also interconnected with other nutrient cycles to maintain an overall metabolic balance in plants, animals, and fungi.[23]
The rapid economic growth, industrialization and urbanization are associated with a strong increase in energy demand and emissions ofair pollutants includingsulfur dioxide (see alsoacid rain) andhydrogen sulfide, which may affect plantmetabolism. Sulfur gases are potentiallyphytotoxic, however, they may also be metabolized and used as sulfur source and even be beneficial if the sulfurfertilization of the roots is not sufficient.
Plant shoots form a sink for atmosphericsulfur gases, which can directly be taken up by the foliage (dry deposition). The foliar uptake of sulfur dioxide is generally directly dependent on the degree of opening of thestomates, since the internal resistance to this gas is low. Sulfite is highly soluble in theapoplastic water of themesophyll, where itdissociates under formation ofbisulfite andsulfite.
Sulfite may directly enter the sulfur reduction pathway and be reduced tosulfide, incorporated into cysteine, and subsequently into other sulfur compounds. Sulfite may also be oxidized tosulfate, extra- and intracellularly byperoxidases or non-enzymatically catalyzed by metal ions orsuperoxideradicals and subsequently reduced and assimilated again. Excessive sulfate is transferred into the vacuole; enhanced foliar sulfate levels are characteristic for exposed plants.The foliar uptake of hydrogen sulfide appears to be directly dependent on the rate of its metabolism into cysteine and subsequently into other sulfur compounds. There is strong evidence that O-acetyl-serine (thiol)lyase is directly responsible for the active fixation of atmospheric hydrogen sulfide by plants.
Plants are able to transfer from sulfate to foliar absorbed atmospheric sulfur as sulfur source and levels of 60ppb or higher appear to be sufficient to cover the sulfur requirement of plants. There is an interaction between atmospheric and pedospheric sulfur utilization. For instance, hydrogen sulfide exposure may result in a decreased activity of APS reductase and a depressed sulfate uptake.
