- Sulfur assimilation
thumb|">Sulfate reduction and assimilation in plants (APS, adenosine 5'-phosphosulfate; Fdred, Fdox, reduced and oxidized ferredoxin; RSH, RSSR, reduced and oxidized glutathione)|right|325px
Sulfur is an essential element for growth andphysiological functioning ofplant s, however, its content strongly varies between plantspecies and it ranges from 0.1 to 6 % of the plants' dry weight.Sulfate taken up by theroot s is the major sulfur source for growth, though it has to be reduced tosulfide before it is further metabolized. Rootplastids contain allsulfate reductionenzymes , however, the reduction of sulfate tosulfide and its subsequent incorporation into cysteine takes predominantly place in the shoot in thechloroplast .Cysteine is the precursor or reduced sulfur donor of most other organic sulfur compounds in plants. The predominant proportion of the organic sulfur is present in theprotein fraction (up to 70 % of total sulfur), as cysteine andmethionine residues. Cysteine and methionine are highly significant in the structure, conformation and function ofproteins . Plants contain a large variety of other organic sulfur compounds, asthiols (glutathione ),sulfolipid s and secondary sulfur compounds (alliin s,glucosinolate s,phytochelatins ), which play an important role inphysiology and protection againstenvironmental stress and pests. Sulfur compounds are also of great importance forfood quality and for the production of phyto-pharmaceutics . Sulfurdeficiency will result in the loss of plant production, fitness and resistance toenvironmental stress and pests.ulfate uptake by plants
Sulfate is taken up by theroot s with high affinity and 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 is strictly controlled and it appears to be one of the primary regulatory sites of sulfur assimilation. Sulfate is actively taken up across theplasma membrane of theroot cells, subsequently loaded into thexylem vessels and transported to the shoot by thetranspiration stream. The uptake and transport of sulfate is energy dependent (driven by aproton gradient generated byATPases ) through a proton/sulfate co-transport. In the shoot the sulfate is unloaded and transported to the chloroplasts where it is reduced. The remaining 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. According to their cellular and subcellulargene expression , and possible functioning the sulfatetransporter sgene family has been classified in up to 5 different groups. Some groups are expressed exclusively in the roots or shoots or expressed both in the roots and shoots. Group 1 are 'high affinity sulfate transporters', which are involved in the uptake of sulfate by the roots. Group 2 are vascular transporters and are 'low affinity sulfate transporters'. Group 3 is the so-called 'leaf group', however, still little is known about the characteristics of this group. Group 4 transporters may be involved in the transport of sulfate into theplastids prior to its reduction, whereas the function of Group 5 sulfate transporters is not known yet. Regulation and expression of the majority of sulfate transporters are controlled by the sulfurnutrition al status of the plants. 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 a substantially enhanced sulfate uptake capacity. It is not yet solved, whether sulfate itself or metabolic products of the sulfur assimilation (O-acetyl-serine ,cysteine ,glutathione ) act as signals in the regulation of sulfate uptake by the root and its transport to the shoot, and in the expression of the sulfate transporters involved.ulfate reduction in plants
Even though
root plastids contain all sulfate reductionenzymes , sulfate reduction takes pre-dominantly place in the leafchloroplast s. The reduction ofsulfate tosulfide occurs in three steps. Sulfate needs to be activated toadenosine 5'-phosphosulfate (APS) prior to its reduction tosulfite . The activation of sulfate is catalyzed by ATP sulfurylase, which affinity for sulfate is rather 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 with likelyglutathione asreductant . 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 by sulfite 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.ynthesis and function of sulfur compounds in plants
Cysteine
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 named cysteine synthase. The formation of cysteine is the direct coupling step between sulfur andnitrogen assimilation in plants. 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 chain s (and formcystine ) and/or linkage ofpolypeptides . Disulfide bridges (disulfide bond s) 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.ferredoxin s) and in regulatory proteins (e.g.thioredoxin s).Glutathione
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. 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. Glutathione is maintained in the reduced form by anNADPH -dependentglutathione reductase and the ratio of reduced glutathione (GSH) to oxidized glutathione (GSSG) generally exceeds a value of 7.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 lipidhydroperoxide s. 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 ofxenobiotic s, 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 distinctisoform s 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 lipidhydroperoxide s, in the conjugation of endogenous metabolites,hormones andDNA degradation products, and in the transport offlavonoids .ulfolipids
Sulfoquinovosyl diacylglycerol is the predominant sulfur-containing
lipid present in plants. In leaves its content comprises up to 3 - 6 % of the total sulfur present. This sulfolipid is present inplastid membranes and likely is involved inchloroplast functioning. The route ofbiosynthesis and physiological function of sulfoquinovosyl diacylglycerol is still under investigation. From recent studies it is evident thatsulfite it the likely sulfur for the formation of the sulfoquinovose group of this lipid.econdary sulfur compounds
Brassica species containglucosinolate s, 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 cysteine) 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 asisothiocyanate s,thiocyanate s,nitrile s 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 andalliin s (S-alk(en)yl cysteine sulfoxides). The content of these sulfur-containingsecondary compound s 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. 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-glutamyltranspeptidase s. 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.Sulfur metabolism in plants and air pollution
The rapid economic growth, industrialization and urbanization are associated with a strong increase in energy demand and emissions of
air pollutant s includingsulfur dioxide (see alsoacid rain ) andhydrogen sulfide , which may affect plantmetabolism . Sulfur gases are potentially phytotoxic , 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. Sulfur is highly soluble in theapoplast ic water of themesophyll , where itdissociate s 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 byperoxidase s or non-enzymatically catalyzed by metal ions orsuperoxide radicals 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.ee also
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Sulphur metabolism Sources
Schnug, E. (1998) Sulfur in Agroecosystems. Kluwer Academic Publishers, Dordrecht, 221 pp, ISBN 0-7923-5123-1.
Grill, D., Tausz, M. and De Kok, L.J. (2001) Significance of Glutathione to Plant Adaptation to the Environment. Kluwer Academic Publishers, Dordrecht, ISBN 1-4020-0178-9.
Abrol Y.P. and Ahmad A. (2003) Sulphur in Plants. Kluwer Academic Publishers, Dordrecht, ISBN 1-4020-1247-0.
Saito, K., De Kok, L.J., Stulen, I., Hawkesford, M.J., Schnug, E., Sirko, A. and Rennenberg, H. (2005) Sulfur Transport and Assimilation in Plants in the Post Genomic Era. Backhuys Publishers, Leiden, ISBN 90-5782-166-4. Hawkesford, M.J. and De Kok, L.J. (2006) Managing sulfur metabolism in plants. Plant Cell and Environment 29: 382-395.
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