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N Use By Plants
Nitrate Assimilation
Ammonia Assimilation
Glu, Gln, Asn, Gly, Ser
Aminotransferases
Asp, Ala, GABA
Val, Leu, Ileu, Thr, Lys
Pro, Arg, Orn
Polyamines
Non-protein AAs
Alkaloids
Sulfate Assimilation
Cys, Met, AdoMet, ACC
His, Phe, Tyr, Tryp
Secondary Products
Onium Compounds
Enzymes
Methods
Simulation
References
HORT640 - Metabolic Plant Physiology

Sulfate uptake and assimilation

Sulfate uptake, reduction and the synthesis of cysteine and methionine in plants

As discussed in the previous pages, the prevailing evidence is that in plants the sulfate assimilation pathway differs from that in other sulfate assimilating organisms; the main pathway of sulfate reduction in plants appears to be via APS rather than PAPS (i.e. APS can be utilized directly, without activation to PAPS, as an intermediary substrate in reductive sulfate assimilation). Sulfite is formed from APS by the action of a glutathione-dependent APS reductase which possesses APS sulfotransferase activity (Bick and Leustek, 1998; Setya et al, 1996; Gutierrez-Marcos et al, 1996; Wray et al, 1998).

Sulfite generated by the catalytic action of APS reductase is reduced to free sulfide by sulfite reductase [EC 1.8.7.1]. A cDNA termed sir has been isolated from Arabidopsis thaliana leaf tissue that is homologous to a ferredoxin-dependent sulfite reductase [EC 1.8.7.1] from Synechococcus PCC7942 and distantly related to the hemoprotein subunit of Escherichia coli NADPH-dependent sulfite reductase [EC 1.8.1.2] (Bruhl et al, 1996). The Arabidopis ferredoxin-dependent sulfite reductase is predicted to have a molecular mass of 71.98 kDa, consisting of 642 amino acids, including a transit peptide of 66 residues (6.72 kDa) that is assumed to direct the protein into the plastid. The truncated cDNA clone (with the transit peptide sequence deleted), expressed as his-tag fusion, yielded a protein that was enzymatically inactive (Bruhl et al, 1996). However, this protein cross-reacted with polyclonal antibodies against ferredoxin sulfite reductase from Synechococcus (Bruhl et al, 1996).

The six-electron reduction of sulfite to sulfide resembles that of the reduction of nitrite to ammonia (Crane and Getzoff, 1996). Sulfite and nitrite reductases share an unusual prosthetic assembly in their active centers, namely siroheme covalently linked to an Fe4S4 cluster (Crane and Getzoff, 1996). The recently determined crystallographic structure of the sulfite reductase hemoprotein from Escherichia coli (Crane et al, 1995) reveals structural features that are key for the catalytic mechanisms and suggest a common symmetric structural unit for this diverse family of enzymes (Crane and Getzoff, 1996).

Siroheme, is a cofactor of both sulfite and nitrite reductase in Salmonella typhimurium, and requires the cysG gene for its synthesis (Goldman and Roth, 1993). Three steps are required to synthesize siroheme from uroporphyrinogen III (a methylated, iron-containing modified tetrapyrrole), the last common intermediate in the heme and siroheme pathways. In Salmonella, cysG mutants are defective in the synthesis of cobalamin (B12), which shares a common precursor with siroheme (Goldman and Roth, 1993). A cysG mutant strain of Rhizobium etli that is pleiotropically defective in sulfate and nitrate assimilation has a mutation in a siroheme synthetase-homologous gene (Tate et al, 1997).

A cDNA (UPM1) was cloned from Arabidopsis thaliana that functionally complements an Escherichia coli cysG mutant that is unable to catalyze the conversion of uroporphyrinogen III to siroheme (Leustek et al, 1997). UPM1 encodes a 369-amino acid, 39.9-kDa protein. The UPM1 product has a sequence at the amino terminus that resembles a transit peptide for localization to mitochondria or plastids. The protein produced by in vitro expression is able to enter isolated intact chloroplasts but not mitochondria (Leustek et al, 1997). The UPM1 product contains two regions that are identical to consensus sequences found in bacterial uroporphyrinogen III and precorrin methyltransferases (Leustek et al, 1997). Recombinant UPM1 protein catalyzes S-adenosyl-L-methionine-dependent transmethylation by UPM1 (Leustek et al, 1997).

A full-length cDNA clone (pZmSUMT1) encoding an S-adenosyl-L-methionine-dependent uroporphyrinogen III C-methyltransferase (SUMT) [EC 2.1.1.107] has also been isolated from a maize root cDNA library (Sakakibara et al, 1996). The deduced amino acid sequence of the open reading frame of the cDNA is similar to that of SUMT from various bacteria and also to the SUMT catalytic region of siroheme synthase (cysG) from Escherichia coli. Overproduction of ZmSUMT1 in a cysG mutant of E. coli eliminated the requirement of the strain for cysteine (Sakakibara et al, 1996). The gene is induced in both roots and leaves in response to the addition of nitrate to the culture medium; the gene product is imported into plastids. ZmSUMT1 might be involved in the synthesis of siroheme, a prosthetic group of both nitrite and sulfite reductase. Gene expression is co-regulated with that of other nitrate-assimilatory genes (Sakakibara et al, 1996).

The incorporation of sulfide into organic form in the biosynthesis of cysteine, represents the final step of sulfate assimilation in bacteria and plants, catalyzed by the sequential action of serine acetyltransferase (SAT) and O-acetylserine (thiol) lyase (OAS-TL). These enzymes form a cysteine synthase (CS) complex both in vitro and in vivo (Bogdanova and Hell, 1997; Wray et al, 1998).

In pea leaves, serine O-acetyltransferase [EC 2.3.1.30] activity is mainly located in mitochondria (approximately 76% of total cellular activity), with significant activity was also identified in both the cytosol (14% of total) and chloroplasts (10% of total) (Ruffet et al, 1995). Three enzyme forms were separated by anion-exchange chromatography, and each form was found to be specific for a given intracellular compartment. Using an Escherichia coli mutant devoid of serine acetyltransferase activity, 3 distinct cDNAs encoding serine acetyltransferase isoforms were isolated from Arabidopsis (Ruffet et al, 1995). One of the isoforms characterized showed none of the general features of transit peptides in the N-terminal region and may represent the cytosolic form (Ruffet et al, 1995).

A cDNA encoding serine acetyltransferase was also cloned from Arabidopsis thaliana (Bogdanova et al, 1995). The plant protein has a predicted molecular weight of 32.8 kDa and shows up to 43% of amino acid homology to bacterial serine acetyltransferases. Moreover, it complements a serine acetyltransferase deficient mutant of E. coli. The mRNA is predominantly expressed in illuminated plant tissue and represents one of at least two related genes (Bogdanova et al, 1995).

Murillo et al (1995) identified at least three genes for serine acetyltransferase in Arabidopsis thaliana. One of these genes, SAT1, encodes a 34-kDa protein that is able to functionally complement a serine acetyltransferase mutant strain of Escherichia coli (Murillo et al, 1995). The predicted amino acid sequence of SAT1 shows significant homology with bacterial serine acetyltransferases. SAT1 protein shows serine acetyltransferase enzyme activity and cross-reacts with an antibody against the E. coli enzyme (Murillo et al, 1995). Although the first 40 amino acids of the SAT1 polypeptide resembles a plastid transit peptide, Murillo et al (1995) conclude that the polypeptide is probably not plastid localized. SAT1 is a single copy gene that is expressed in both leaves and roots (Murillo et al, 1995). Roberts and Wray (1996) also cloned an Arabidopsis thaliana cDNA encoding serine acetyltransferase by functional complementation of the Escherichia coli cysE mutant. The cDNA clone Sat-1 conferred serine acetyltransferase activity on the cysE mutant (Roberts and Wray, 1996). The full-length cDNA encodes a deduced protein of 391 amino acids which includes a putative chloroplastic targeting presequence (Roberts and Wray, 1996).

cDNAs encoding for two isoforms of O-acetylserine (thiol) lyase (OAS-TL) have been isolated from Arabidopsis thaliana (Hell et al, 1994). One isoform is localized in the cytosol and the other in the plastids. The cytosolic OAS-TL complemented an E. coli auxotrophic mutant lacking cysteine synthesis. Both isoforms are represented by small gene families. Expression is increased in response to limited sulfate supply (Hell et al, 1994). A third cDNA, Atcys-3A, encoding OAS-TL was isolated from Arabidopsis by Barroso et al (1995). This cDNA shows a high level of similarity with the bacterial counterpart, and a other higher plant OAS-TL genes (Barroso et al, 1995). Atcys-3A expression was also activated by sulfur limitation, requiring a carbon and nitrogen source for maximal expression (Barroso et al, 1995).

Several isoforms of cysteine synthase (O-acetylserine sulfhydrylase; OASS [EC 4.2.99.8]) have been detected in other plants; cytoplasmic (encoded by CysA), chloroplastic/plastidic (encoded by CysB) and mitochondrial (encoded by CysC) (Saito et al, 1992; Takahashi and Saito, 1996). In sulfur-starved cells of spinach only small increases in mRNA levels of CysA and CysB were observed. However, under nitrogen and nitrogen/sulfur double-deficient stress conditions (but not under sulfur starvation alone), mRNA levels of CysC increased 500% within 72 h (Takahashi and Saito, 1996).

In Datura innoxia 3 isoforms of O-acetylserine sulfhydrylase (cysteine synthase) are also found; a chloroplast form (most abundant in green leaves), a cytosolic form (abundant in roots and cell cultures), and a mitochondrial form (abundant in cell cultures, but a minor constituent in leaves and roots) (Kuske et al, 1996). Cadmium-tolerant cell cultures have an ~2-fold elevated level of OASS (Kuske et al, 1996).

A cDNA clone (CGS1) cystathionine gamma-synthase [EC 4.2.99.9] (CGS) from Arabidopsis thaliana was selected by functional complementation of a CGS mutant strain of Escherichia coli (metB) (Kim and Leustek, 1996). A single gene homologous with CGS1 is present in the A. thaliana genome. CGS1 encodes a 563 amino acid, 60 kDa protein. The predicted amino acid sequence contains a consensus pyridoxal phosphate-binding site and is similar to MetB of E. coli (Kim and Leustek, 1996). The CGS1 product has a sequence at the amino terminus that resembles a transit peptide for localization to plastids (Kim and Leustek, 1996). Repression of CGS in Arabidopsis produces partial methionine auxotrophy and developmental abnormalities (Kim and Leustek, 2000).

Note that in humans, cystathionine is synthesized by cystathionine beta-synthase; an unusual enzyme that requires the cofactors heme and pyridoxal phosphate (PLP) to catalyze the condensation of homocysteine and serine to generate cystathionine (Taoka et al, 1999). This transsulfuration reaction represents one of two major cellular routes for detoxification of homocysteine, which is a risk factor for atherosclerosis (Taoka et al, 1999). In the inborn error of metabolism, homocystinuria (hyperhomocysteinemia) due to cystathionine beta-synthase deficiency, there is greatly increased circulating homocyst(e)ine and a clear association with precocious vascular disease (Dudman et al, 1996; Fowler, 1997; Wilcken and Wilcken, 1998).

Cystathionine beta-lyase (B-Cystathionase) [EC 4.4.1.8] catalyses the synthesis of homocysteine from cystathionine; a cDNA encoding cystathionine beta-lyase has been cloned from Arabidopsis thaliana complementation of an Escherichia coli mutant deficient in this enzyme (Ravanel et al, 1995). The nucleotide sequence encodes a polypeptide of 464 amino acids (50.37 kDa) (Ravanel et al, 1995), A. thaliana cystathionine beta-lyase exhibits 22% sequence identity with the E. coli corresponding enzyme, and contains a 70 amino acid N-terminal sequence with the general features of chloroplast transit peptides, suggesting a chloroplast localization of the enzyme (Ravanel et al, 1995). Southern blot analysis suggests that cystathionine beta-lyase is encoded by a single copy gene in A. thaliana (Ravanel et al, 1995). Transgenic potato plants expressing antisense cystathionine beta-lyase show reduced methionine levels and increased levels of cystathionine, homoserine, cysteine and homocysteine, associated with a bushy growth habit, small light-green leaves and small tubers (Maimann et al, 2000). Levels of aspartate, lysine and threonine were unaffected (Maimann et al, 2000). The bushy phenotype is alleviated by supplementation with methionine, suggesting that low methionine levels (rather than pathway intermediate accumulation) is responsible for the phenotypic effects.

The reaction catalyzed by cobalamin-dependent methionine synthase (5-methyltetrahydrofolate:homocysteine methyltransferase) [EC 2.1.1.13] of Escherichia coli involves the transfer of a methyl group from methyltetrahydrofolate to homocysteine to generate tetrahydrofolate and methionine (Frasca et al, 1988; Banerjee et al, 1990ab). The cobalamin-dependent methionine synthase of E. coli is encoded by the MetH gene (Goulding and Matthews, 1997). The reaction mechanism is thought to involve an initial transfer of the methyl group to the enzyme to generate enzyme-bound methylcobalamin and tetrahydrofolate. Enzyme-bound methylcobalamin then donates its methyl group to homocysteine to generate methionine and cob(I)alamin (Banerjee et al, 1990ab; Banerjee and Matthews, 1990). Enzyme possessing cobalamin in the cobalt(II) oxidation state is inactive, and this form is activated by a one-electron reduction coupled to methylation by S-adenosylmethionine (AdoMet) (Drummond et al, 1993a). The electron is supplied by reduced flavodoxin (Hoover et al, 1997). The E. coli enzyme is a monomeric 136.1-kDa enzyme (Drummond et al, 1993b). The protein has at least four distinct regions; amino acids 2-353 comprise a region responsible for binding and activation of homocysteine, amino acids 345-649 are thought to be involved in the binding and activation of methyltetrahydrofolate, amino acids 650-896 are responsible for binding of the prosthetic group methylcobalamin, and amino acids 897-1227 are involved in binding S-adenosylmethionine and are required for reductive activation of enzyme in the cob(II)alamin form (Goulding and Matthews, 1997; Goulding et al, 1997). Zinc is involved in homocysteine activation (Goulding and Matthews, 1997).

Mammalian methionine synthase is also cobalamin-dependent (Chen et al, 1994). The mammalian enzyme from pig liver is a large monomeric protein with a molecular mass of 151-155 kDa. It is characterized by the absence of any metals other than cobalt which is associated with the cofactor, cobalamin (Chen et al, 1994). Like the cobalamin-dependent methionine synthase from Escherichia coli the mammalan enzyme is dependent on S-adenosylmethionine for activity (Chen et al, 1994).

In addition to the cobalamin-dependent methionine synthase, Escherichia coli has a cobalamin-independent methionine synthase (MetE) [EC 2.1.1.14] that catalyzes the transfer of a methyl group from methyltetrahydrofolate to homocysteine (Gonzalez et al, 1996). A reactive thiol group, cysteine 726, is required for catalytic activity. The enzyme is a zinc metalloenzyme containing ~1 equivalent of zinc per subunit; cysteine 726 is required for metal binding (Gonzalez et al, 1996). The cobalamin-independent methionine synthase shares no similarity with the sequence of the cobalamin-dependent protein, suggesting that the two have arisen by convergent evolution (Gonzalez et al, 1992). Note that higher plants only possess the cobalamin-independent methionine synthase [EC 2.1.1.14].

The biosynthesis of methionine in Escherichia coli is under complex regulation. The repression of the biosynthetic pathway by methionine is mediated by a repressor protein (MetJ protein) and S-adenosyl-methionine which functions as a corepressor for the MetJ protein (Weissbach and Brot, 1991). A regulatory protein, MetR, protein is required for both metE and metH gene expression, and functions as a transactivator of transcription of these genes. MetR is a transcription activator that possesses a leucine zipper motif (Weissbach and Brot, 1991). The transcriptional activity of MetR is modulated by homocysteine, the metabolic precursor of methionine (Weissbach and Brot, 1991). Vitamin B12 can repress expression of the metE gene. This effect is mediated by the MetH holoenzyme, which contains a cobamide prosthetic group (Weissbach and Brot, 1991).

For recent reviews of sulfur amino acid biosynthesis and its regulation in plants, see: Saito (1999), Saito (2000) and Leustek et al (2000).

References

Banerjee RV, Frasca V, Ballou DP, Matthews RG 1990a Participation of cob(I)alamin in the reaction catalyzed by methionine synthase from Escherichia coli: a steady-state and rapid reaction kinetic analysis. Biochemistry 29: 11101-11109.

Banerjee RV, Harder SR, Ragsdale SW, Matthews RG 1990b Mechanism of reductive activation of cobalamin-dependent methionine synthase: an electron paramagnetic resonance spectroelectrochemical study. Biochemistry 29: 1129-1135.

Banerjee RV, Matthews RG 1990 Cobalamin-dependent methionine synthase. FASEB J. 4: 1450-1459.

Barroso C, Vega JM, Gotor C 1995 A new member of the cytosolic O-acetylserine(thiol)lyase gene family in Arabidopsis thaliana. FEBS Lett. 363: 1-5.

Bick JA, Leustek T 1998 Plant sulfur metabolism--the reduction of sulfate to sulfite. Curr. Opin. Plant Biol. 1: 240-244.

Bogdanova N, Bork C, Hell R 1995 Cysteine biosynthesis in plants: isolation and functional identification of a cDNA encoding a serine acetyltransferase from Arabidopsis thaliana. FEBS Lett. 358: 43-47.

Bogdanova N, Hell R 1997 Cysteine synthesis in plants: protein-protein interactions of serine acetyltransferase from Arabidopsis thaliana. Plant J. 11: 251-262.

Bruhl A, Haverkamp T, Gisselmann G, Schwenn JD 1996 A cDNA clone from Arabidopsis thaliana encoding plastidic ferredoxin:sulfite reductase. Biochim. Biophys. Acta 1295: 119-124.

Chen Z, Crippen K, Gulati S, Banerjee R 1994 Purification and kinetic mechanism of a mammalian methionine synthase from pig liver. J. Biol. Chem. 269: 27193-27197.

Crane BR, Getzoff ED 1996 The relationship between structure and function for the sulfite reductases. Curr. Opin. Struct. Biol. 6: 744-756.

Crane BR, Siegel LM, Getzoff ED 1995 Sulfite reductase structure at 1.6 A: evolution and catalysis for reduction of inorganic anions. Science 270: 59-67.

Drummond JT, Huang S, Blumenthal RM, Matthews RG 1993a Assignment of enzymatic function to specific protein regions of cobalamin-dependent methionine synthase from Escherichia coli. Biochemistry 32: 9290-9295.

Drummond JT, Loo RR, Matthews RG 1993b Electrospray mass spectrometric analysis of the domains of a large enzyme: observation of the occupied cobalamin-binding domain and redefinition of the carboxyl terminus of methionine synthase. Biochemistry 32: 9282-9289.

Dudman NP, Guo XW, Gordon RB, Dawson PA, Wilcken DE 1996 Human homocysteine catabolism: three major pathways and their relevance to development of arterial occlusive disease. J. Nutr. 126: 1295S-1300S.

Fowler B 1997 Disorders of homocysteine metabolism. J. Inherit. Metab. Dis. 20: 270-285.

Frasca V, Banerjee RV, Dunham WR, Sands RH, Matthews RG 1988 Cobalamin-dependent methionine synthase from Escherichia coli B: electron paramagnetic resonance spectra of the inactive form and the active methylated form of the enzyme. Biochemistry 27: 8458-8465.

Goldman BS, Roth JR 1993 Genetic structure and regulation of the cysG gene in Salmonella typhimurium. J. Bacteriol. 175: 1457-1466.

Gonzalez JC, Banerjee RV, Huang S, Sumner JS, Matthews RG 1992 Comparison of cobalamin-independent and cobalamin-dependent methionine synthases from Escherichia coli: two solutions to the same chemical problem. Biochemistry 31: 6045-6056.

Gonzalez JC, Peariso K, Penner-Hahn JE, Matthews RG 1996 Cobalamin-independent methionine synthase from Escherichia coli: a zinc metalloenzyme. Biochemistry 35: 12228-12234.

Goulding CW, Matthews RG 1997 Cobalamin-dependent methionine synthase from Escherichia coli: involvement of zinc in homocysteine activation. Biochemistry 36: 15749-15757.

Goulding CW, Postigo D, Matthews RG 1997 Cobalamin-dependent methionine synthase is a modular protein with distinct regions for binding homocysteine, methyltetrahydrofolate, cobalamin, and adenosylmethionine. Biochemistry 36: 8082-8091.

Gutierrez-Marcos JF, Roberts MA, Campbell EI, Wray JL 1996 Three members of a novel small gene-family from Arabidopsis thaliana able to complement functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and "APS reductase" activity. Proc. Natl. Acad. Sci. U.S.A. 93: 13377-13382.

Hell R, Bork C, Bogdanova N, Frolov I, Hauschild R 1994 Isolation and characterization of two cDNAs encoding for compartment specific isoforms of O-acetylserine (thiol) lyase from Arabidopsis thaliana. FEBS Lett. 351: 257-262.

Hoover DM, Jarrett JT, Sands RH, Dunham WR, Ludwig ML, Matthews RG 1997 Interaction of Escherichia coli cobalamin-dependent methionine synthase and its physiological partner flavodoxin: binding of flavodoxin leads to axial ligand dissociation from the cobalamin cofactor. Biochemistry 36: 127-138.

Kim J, Leustek T 1996 Cloning and analysis of the gene for cystathionine gamma-synthase from Arabidopsis thaliana. Plant Mol. Biol. 32: 1117-1124.

Kim J, Leustek T 2000 Repression of cystathionine gamma-synthase in Arabidopsis thaliana produces partial methionine auxotrophy and developmental abnormalities. Plant Sci. 151: 9-18.

Kuske CR, Hill KK, Guzman E, Jackson PJ 1996 Subcellular location of O-acetylserine sulfhydrylase isoenzymes in cell cultures and plant tissues of Datura innoxia Mill. Plant Physiol. 112: 659-667.

Leustek T, Martin MN, Bick JA, Davies JP 2000 Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51: 141-165.

Leustek T, Smith M, Murillo M, Singh DP, Smith AG, Woodcock SC, Awan SJ, Warren MJ 1997 Siroheme biosynthesis in higher plants. Analysis of an S-adenosyl-L-methionine-dependent uroporphyrinogen III methyltransferase from Arabidopsis thaliana. J. Biol. Chem. 272: 2744-2752.

Maimann S, Wagner C, Kreft O, Zeh M, Willmitzer L, Hofgen R, Hesse H 2000 Transgenic potato plants reveal the indispensable role of cystathionine beta-lyase in plant growth and development. Plant J. 23: 747-758.

Murillo M, Foglia R, Diller A, Lee S, Leustek T 1995 Serine acetyltransferase from Arabidopsis thaliana can functionally complement the cysteine requirement of a cysE mutant strain of Escherichia coli. Cell Mol. Biol. Res. 41: 425-433.

Ravanel S, Ruffet ML, Douce R 1995 Cloning of an Arabidopsis thaliana cDNA encoding cystathionine beta-lyase by functional complementation in Escherichia coli. Plant Mol. Biol. 29: 875-882.

Roberts MA, Wray JL 1996 Cloning and characterization of an Arabidopsis thaliana cDNA clone encoding an organellar isoform of serine acetyltransferase. Plant Mol. Biol. 30: 1041-1049.

Ruffet ML, Lebrun M, Droux M, Douce R 1995 Subcellular distribution of serine acetyltransferase from Pisum sativum and characterization of an Arabidopsis thaliana putative cytosolic isoform. Eur. J. Biochem. 227: 500-509.

Sakakibara H, Takei K, Sugiyama T 1996 Isolation and characterization of a cDNA that encodes maize uroporphyrinogen III methyltransferase, an enzyme involved in the synthesis of siroheme, which is prosthetic group of nitrite reductase. Plant J. 10: 883-892.

Saito K 1999 Biosynthesis of cysteine. In (BK Singh ed.) "Plant Amino Acids: Biochemistry and Biotechnology", Marcel Dekker, NY, pp. 267-291.

Saito K 2000 Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr. Opin. Plant Biol. 3: 188-195.

Saito K, Miura N, Yamazaki M, Hirano H, Murakoshi I 1992 Molecular cloning and bacterial expression of cDNA encoding a plant cysteine synthase. Proc. Natl. Acad. Sci. U.S.A. 89: 8078-8082.

Setya A, Murillo M, Leustek T 1996 Sulfate reduction in higher plants: molecular evidence for a novel 5'-adenylylsulfate reductase. Proc. Natl. Acad. Sci. U.S.A. 93: 13383-13388.

Takahashi H, Saito K 1996 Subcellular localization of spinach cysteine synthase isoforms and regulation of their gene expression by nitrogen and sulfur. Plant Physiol. 112: 273-280.

Taoka S, West M, Banerjee R 1999 Characterization of the heme and pyridoxal phosphate cofactors of human cystathionine beta-synthase reveals nonequivalent active sites. Biochemistry 38: 2738-2744.

Tate R, Riccio A, Iaccarino M, Patriarca EJ 1997 A cysG mutant strain of Rhizobium etli pleiotropically defective in sulfate and nitrate assimilation. J. Bacteriol. 179: 7343-7350.

Weissbach H, Brot N 1991 Regulation of methionine synthesis in Escherichia coli. Mol. Microbiol. 5: 1593-1597.

Wilcken DE, Wilcken B 1998 B vitamins and homocysteine in cardiovascular disease and aging. Ann. N. Y. Acad. Sci. 854: 361-370.

Wray JL, Campbell EI, Roberts MA, Gutierrez-Marcos JF 1998 Redefining reductive sulfate assimilation in higher plants: a role for APS reductase, a new member of the thioredoxin superfamily? Chem. Biol. Interact. 109: 153-167.

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