Biosynthesis of Serine, Glycine, and One-Carbon Units
Chapter
30
GEORGE V. STAUFFER
The biosynthesis of serine, glycine and one-carbon (C1) units has been the subject of numerous studies (41, 56, 88, 92, 93). During growth on glucose, 15% of the carbon assimilated in Escherichia coli involves serine or its metabolites (69). Serine is used in the synthesis of cysteine, tryptophan, and phospholipids, and glycine is a precursor of purines and heme-containing compounds (5, 39, 69). C1 units are used in the synthesis of purines, histidine, thymine, methionine, the formylation of aminoacylated initiator tRNA, and S-adenosylmethionine (SAM) (5). SAM is a methyl donor used in the methylation of DNA (43), the modification of tRNA (57), and the methylation of proteins involved in chemotaxis (84) and other cytoplasmic proteins (38). In addition, C1 limitation is responsible for an altered heat shock response (27). Thus, the biosynthesis of serine, glycine, and C1 units constitutes a major metabolic pathway that plays a central role in cell physiology.
The serine, glycine and C1 pathway in E. coli and Salmonella typhimurium (official designation, Salmonella enterica serovar Typhimurium) is shown in Fig. 1 (67, 118, 119). The glycolytic intermediate 3-phosphoglycerate is converted to serine in three steps. 3-Phosphoglycerate dehydrogenase (serA gene product) oxidizes 3-phosphoglycerate to 3-phosphohydroxypyruvate, the first committed step in the pathway. 3-Phosphoserine aminotransferase (serC gene product) converts 3-phosphohydroxypyruvate to 3-phosphoserine. This enzyme is also required for the biosynthesis of pyridoxine (14, 15, 89). 3-Phosphoserine is dephosphorylated to l-serine by 3-phosphoserine phosphatase (serB gene product). Serine is converted to glycine and a C1 unit by serine hydroxymethyltransferase (SHMT) (glyA gene product) (90, 95); the C1 unit is captured as a methylene group transferred to the cofactor tetrahydrofolate, forming 5,10-methylene tetrahydrofolate.
The final step in the pathway is the oxidative cleavage of glycine to NH3, CO2, and 5,10-methylene tetrahydrofolate by the glycine cleavage (GCV) enzyme system (52, 65, 70, 99, 102). The GCV enzyme system in plants, animals, and bacteria is composed of four protein components (41). P protein (gcvP gene product) catalyzes the decarboxylation of glycine to CO2 and an aminomethyl group (36). H protein (gcvH gene product), which contains a covalently bound lipoic acid prosthetic group (25, 126), serves as an electron sink and as a carrier of the aminomethyl moiety derived from glycine (36). T protein (encoded by gcvT) is involved in the transfer of the C1 unit from H protein to tetrahydrofolate and the release of NH3 (26). The reduced lipoic acid of the H protein is reoxidized by the L protein to the disulfide form (55). The lpd-encoded lipoamide dehydrogenase, common to the pyruvate and 2-oxoglutarate dehydrogenase multienzyme complexes, functions as the L protein in the GCV enzyme complex (108).
Mutations in the serine pathway result in a requirement that can be met from either exogenous serine or glycine via the SHMT reaction (Fig. 1) (67, 119). Mutations that inactivate SHMT, however, result in a requirement that can only be met by exogenous glycine, demonstrating that serine is the normal precursor of glycine. Loss of the GCV pathway does not result in an auxotrophy (70). However, mutants blocked in both the serine pathway and the GCV pathway cannot use glycine as a serine source, as the GCV reaction accounts for the C1 units required for serine synthesis under this condition (65, 70). E. coli mutants with no detectable GCV activity excrete glycine (28, 70), suggesting that an excess of glycine is produced when all C1 units needed by the cell are produced by the SHMT reaction. Thus, the GCV activity probably maintains appropriate glycine and C1 concentrations by converting the excess glycine to C1 units.
The utilization of threonine constitutes a secondary pathway for serine and glycine biosynthesis. Threonine is converted to glycine and acetyl coenzyme A by a two-step pathway initiated by threonine dehydrogenase (24, 54, 63, 76, 77, 78). The GCV enzyme system then converts glycine to a C1 unit, and SHMT catalyzes the condensation of a C1 unit with a second molecule of glycine to produce serine. The genes encoding the enzymes for threonine utilization are members of the Lrp regulon and are induced by leucine (22, 117), explaining the increased efficiency of threonine oxidation in the presence of leucine (1, 63).
High levels of serine in the growth medium lead to a growth inhibition that is relieved by the addition of isoleucine (10, 124, 125). The growth inhibition is exacerbated by the addition of glycine, methionine, and leucine to the medium or by elevated temperature (10, 12, 33, 125), owing in part to an elevated rate of serine catabolism to pyruvate induced by these agents (37, 46, 49, 50). Elevation of pyruvate leads to isoleucine restriction (3). In addition, leucine represses ilvIH (13), the product of which is the acetohydroxy acid synthase isozyme (AHAS III), which is more effective in the synthesis of isoleucine than the other isoenzyme (AHAS I) normally present in K-12 strains of E. coli.
3-Phosphoglycerate dehydrogenase, the first enzyme of the serine pathway, is feedback inhibited by l-serine (50% inhibition at 4 × 10–5 M) (19, 67, 110, 116, 119) through a conformational change in the enzyme (18, 111). A mutant producing 3-phosphoglycerate dehydrogenase that is resistant to serine inhibition overproduces serine (116). The fact that the intracellular concentrations of 3-phosphoglycerate and serine remain constant in cells with 10-fold differences in 3-phosphoglycerate dehydrogenase activity indicates that end product inhibition of 3-phosphoglycerate dehydrogenase activity is an effective form of control of metabolic flow of carbon through the serine-glycine pathway.
There is no evidence for inhibition of 3-phosphoserine aminotransferase activity, and inhibition of 3-phosphoserine phosphatase by l-serine is 1,000 times less sensitive than is inhibition of 3-phosphoglycerate dehydrogenase (67, 119). Feedback inhibition of SHMT activity could not be demonstrated in either S. typhimurium or E. coli by several compounds involved in C1 metabolism (d-serine, α-methylserine, l-methionine, l-threonine, SAM, purines, and thymine) (47, 91; G. V. Stauffer, Ph.D. thesis, Pennsylvania State University, University Park, 1976).
The enzymes of serine biosynthesis are not regulated by a conventional induction or repression mechanism in response to the levels of serine, seryl-tRNA, or seryl-tRNA synthetase (51, 67, 68, 116, 119). 3-Phosphoglycerate dehydrogenase levels are reduced 10-fold in cells grown in minimal medium with lactate as the carbon source and supplemented with amino acids not directly related to serine biosynthesis (threonine, methionine, leucine, isoleucine) (51, 60). The 3-phosphoglycerate dehydrogenase levels are also negatively regulated by cyclic AMP, and this effect is abolished in a crp mutant (51). 3-Phosphoserine aminotransferase and 3-phosphoserine phosphatase levels remain constant under similar growth conditions.
The leucine-responsive regulatory protein (Lrp) is a global regulatory protein involved in the control of transcription of numerous genes relating to amino acid metabolism (8, 62; see chapter 92). The serA gene is regulated by Lrp and leucine, repressed about fivefold in lrp::Tn10 mutants, and repressed twofold by leucine supplementation (80, 117). Since the proposed target site for Lrp is absent from the serA promoter and because the effects of leucine and Lrp on serA expression are relatively small compared with their effects on other genes or operons of the leucine regulon, Lrp might act indirectly on the serA promoter (80).
The serB gene is divergently transcribed from smp, encoding a membrane protein of unknown function (59), and is cotranscribed with sms (sensitivity to methylmethane sulfonate), which has no apparent role in serine biosynthesis (61). The serC gene is cotranscribed with aroA (21), the product of which is necessary for chorismate synthesis. The conditions and mechanisms to regulate these complex operons remain to be determined. However, transcriptional linkage between genes encoding proteins with unrelated functions may serve to coordinate different metabolic pathways during growth.
Since the SHMT reaction is the major source of glycine and C1 units for cell metabolism (56), one might expect that the cell would regulate the level of this enzyme as environmental conditions change. Indeed, a number of compounds of C1 metabolism (serine, glycine, methionine, purines, pyrimidines) have been reported to alter glyA gene expression (23, 29, 47, 53, 73, 94, 113).
Glycine represses SHMT synthesis (53), but not by the functional state of glycyl-tRNA synthetase or the level of glycyl-tRNA (23). Repression of glyA by C1 compounds occurs even when a condition of glycine limitation is produced (95, 97), suggesting that glycine is not solely responsible for regulation of the glyA gene. Derepression of glyA also occurs when serine-glycine auxotrophs are grown in a serine-limited chemostat culture (16). Again, the addition of purines to these cultures reduces gene expression.
Purine limitation results in derepression of SHMT in both E. coli and S. typhimurium (16, 53, 94, 98). PurR, a repressor protein in purine nucleotide synthesis (42, 83), was shown to be involved in glyA regulation in E. coli (106). PurR binds to a 24-bp region centered 59 to 60 bp upstream of the glyA –35 promoter region (Fig. 2). Hypoxanthine and guanine, corepressors for PurR-mediated regulation of the pur regulon, increased binding of PurR to glyA operator DNA (105). Mutations that changed the PurR-binding sequence away from the consensus sequence increased glyA expression about twofold, and mutations that changed the binding sequence toward the consensus sequence had no significant effect on either PurR-binding or purine-mediated repression (105). Therefore, it may be the position of the PurR-binding site relative to the glyA promoter that is the major determinant of PurR-mediated repression for the glyA gene. Since the products of the SHMT reaction are used in a number of biosynthetic pathways, the narrow range of PurR-mediated repression would allow sufficient levels of C1 units and glycine even in the presence of repressing levels of purines.
The 16-bp PurR-binding site in E. coli and its location relative to the –35 region are conserved in S. typhimurium (107). Since purine supplementation represses the S. typhimurium glyA gene, the mechanism of glyA regulation by purines in this organism is most likely the same as for E. coli.
Purine limitation is of interest since 5-amino 4-imidazole carboxamide riboside 5'-triphosphate (ZTP) is formed from an intermediate in purine biosynthesis. ZTP was proposed as a presumptive alarmone for C1-folate deficiency (6). Alarmones are postulated as signal molecules coupled to various stress conditions and serve to rebalance cell metabolism in response to those conditions. If ZTP is an alarmone that signals C1-folate deficiency, its metabolism could be related to the regulation of the glyA gene. However, in E. coli a folate stress regulon controlled by ZTP could not be demonstrated by two-dimensional electrophoretic resolution (82), suggesting that ZTP may not serve as an alarmone to mediate a physiologically beneficial response to folate stress.
The glyA gene is derepressed in metE and metF mutants during methionine limitation, but not in metA and metB mutants (16, 17, 29, 47). When the intracellular concentrations of sulfur-containing amino acids and nucleosides were measured in methionine-limited chemostat cultures, there was a high correlation between the ratio of homocysteine to SAM and the rate of SHMT synthesis, suggesting that homocysteine is an inducer and SAM is a corepressor for glyA expression (17). Recently, MetR, a LysR family protein required for metE and metH expression (123), was shown to activate the glyA gene two- to fourfold, with homocysteine serving as the coactivator (73). This finding provided explanations for several unanswered questions concerning the methionine involvement in glyA expression. Homocysteine is not produced in metA and metB mutants grown on limiting methionine, except at low levels by a circular pathway from SAM (20). This level is kept low by conversion of homocysteine to methionine since these mutants would have adequate 5-methyltetrahydrofolate levels and homocysteine transmethylase activity. On the other hand, homocysteine would be expected to accumulate in metE and metF mutants because the nonfolate branch of the methionine pathway is operational, but transmethylation of homocysteine cannot occur. Thus, if homocysteine is the coactivator for glyA gene expression, higher levels of SHMT in metE and metF mutants than in metA and metB mutants would be expected.
Both metK and metJ mutations prevent a complete repression of SHMT levels, but only metK mutations result in elevated SHMT levels (29, 52, 96). The metJ gene specifies the aporepressor for the methionine pathway, and the metK gene product, SAM synthetase, catalyzes the synthesis of SAM, the corepressor for MetJ (85). Since the MetJ protein and SAM repress metR (121), SAM probably has an indirect effect on glyA expression by reducing the level of MetR. In metJ mutants (and probably metK mutants), there are elevated levels of MetR protein. Thus, the difference between glyA gene expression in metK and that in metJ mutants is most likely due to the endogenous levels of the coactivator homocysteine in these strains. In metK mutants, in which the conversion of methionine to SAM is blocked, there is likely to be an accumulation of intermediates in the methionine pathway, including homocysteine. High MetR and homocysteine levels would result in elevated SHMT levels. In metJ mutants, all of the met genes are overexpressed, and intermediates in the methionine pathway are probably low because of conversion to methionine and SAM. Thus, the glyA gene is not expressed at a high level, but its complete repression by C1 compounds normally observed is prevented.
MetR binds to two sites centered 121 and 143 bp upstream of the glyA transcription start site (Fig. 2); mutations that change either binding site away from the MetR consensus binding sequence prevent MetR-mediated activation of the glyA gene, and mutations that change the binding sites toward consensus increase MetR-mediated activation of the glyA gene (46a). Other genes regulated by MetR have binding sites that are adjacent to or overlap the promoter sequence (7, 11, 48, 122), suggesting that the mechanism of activation of glyA by MetR could be different from the met genes.
Repression of glyA by purines occurs in a metR mutant as well as metR + strains (73, 105). However, when either the PurR-binding site for glyA or the PurR repressor is inactivated, glyA expression is no longer dependent on MetR activation (105). Furthermore, in purine-limited chemostat cultures the levels of SHMT were not altered by methionine addition (16). Thus, it is possible that the MetR protein interferes with PurR-mediated repression of the glyA gene. The mechanism of interference is unknown. A direct interaction between MetR and PurR would require some degree of DNA bending since the two MetR-binding sites in the glyA control region are centered 121 and 143 bp upstream of +1 and do not overlap the PurR-binding site centered 59 to 60 bp upstream of +1 (Fig. 2). MetR binding at the glyA promoter results in DNA bending at an angle of about 33° (E. Lorenz and G. V. Stauffer, unpublished data). It is possible that bending of the DNA is part of the mechanism of MetR activation of glyA, possibly by allowing an appropriate MetR-PurR interaction to occur or by altering the conformation of the DNA to alter PurR binding.
Trimethoprim supplementation also leads to derepression of SHMT in both E. coli and S. typhimurium (16, 94, 98). In metR mutants, however, the derepressed SHMT level is significantly lower than that in the wild-type strain (73). Since trimethoprim reduces the level of tetrahydrofolate and its derivatives (4), it should block the synthesis of 5-methyltetrahydrofolate from the folate branch of the methionine pathway, but should not block homocysteine production from the nonfolate branch of the pathway. If homocysteine accumulates when trimethoprim is added to the growth medium, part of the increase in SHMT synthesis could be explained as the result of increased MetR-mediated activation of glyA expression. In addition, part of the derepression is likely due to a limitation of the supply of purines when trimethoprim is added to the growth medium (16).
A final control point for glyA gene expression is mRNA stability. The E. coli glyA gene produces a monocistronic mRNA with a 182-nucleotide-long 3' nontranslated region containing two repetitive extragenic palindromic sequences and a rho-independent transcription terminator (75). Either of the two repetitive extragenic palindromic sequences or the transcription terminator is essential to maintain normal glyA mRNA stability by blocking the 3' to 5' exonucleolytic activities of polynucleotide phosphorylase and RNase II (72, 74).
Additional mutants have been isolated from both E. coli and S. typhimurium with increased levels of SHMT (97; Lorenz and Stauffer, unpublished data). Preliminary results indicate that altered regulation in these strains cannot be accounted for by defects in the known regulators of glyA (MetR or PurR) (46a, 73, 105, 106) and suggest that additional factors are likely to be involved in the control of the glyA gene.
It is becoming evident that the gcv operon is a highly regulated system. Since the GCV enzyme complex is important for balancing the cells’ glycine and C1 requirements, an integrated mechanism for sensing and responding to the levels of certain metabolic intermediates and end products would be expected for gcv. A preliminary study showed that growth of serine auxotrophs of E. coli in a medium containing serine and a purine base resulted in a temporary inability of the cells to grow upon transfer to a medium containing only glycine, presumably owing to their inability to obtain C1 units from glycine (64). Thus, formation of the GCV enzymes may be repressed under this condition. Addition of glycine to the repressing medium overcomes the repressive effect of the purine base and allows growth immediately upon transfer to medium containing only glycine, suggesting that glycine induces the GCV enzyme system. This idea was supported by the observation that induction of the GCV enzyme system by glycine was not blocked by the addition of adenine, methionine, and SAM to the growth medium (52). Recently, the gcvA gene was shown to encode a positively acting regulatory protein that increases expression of a gcvT-lacZ fusion about 9-fold when cells are grown in the presence of glycine and causes a 10-fold reduction in the basal level of expression of a gcvT-lacZ fusion when cells are grown in the presence of inosine and the absence of the inducer glycine (130, 131). The results suggest a dual role for the GcvA protein as both an activator in the presence of glycine and a repressor in the presence of inosine.
A second mechanism of purine-mediated regulation of gcv, independent of the gcvA gene product, results in a twofold reduction in the glycine-induced GCV enzyme levels (130). This twofold repression, mediated by the PurR repressor, was also seen by measuring β-galactosidase levels in cells carrying a gcvT-lacZ gene fusion (103). Biochemical and genetic studies identified a PurR-binding site, from about nucleotides –3 to +17 relative to the transcription initiation site in the gcvT promoter region, suggesting a direct involvement of PurR in gcv regulation (Fig. 3) (130). The identity to the consensus sequence at only 12 of 16 bp probably results in the narrow range of PurR-mediated regulation.
As stated above, the GcvA-mediated inosine repression can normally be overcome by the addition of exogenous glycine (130). In a gcv mutant carrying a λ gcvT-lacZ fusion, endogenously produced glycine accumulates in the cell and induces the gcvT-lacZ fusion 10-fold. However, when grown in the presence of inosine, induction of gcv is reduced 10-fold, even though high levels of glycine are present in the cell (A. C. Ghrist and G. V. Stauffer, Abstr. 94th Gen. Meet. Am. Soc. Microbiol. 1994, abstr. H-29, p. 205). Similar results have been reported with a λ placMu phage inserted into gcv (45). Starting with a gcv strain lysogenized with a λ gcvT-lacZ phage, a mutant which displays only a twofold repression of gcvT-lacZ in the presence of inosine was isolated. Complementation and transduction studies suggest that this mutation is not in gcvA, purR, or lrp (see below), genes encoding proteins known to regulate gcv expression. The results suggest that at least one additional factor is involved in purine-mediated regulation of the gcv operon.
The gcvA gene has been cloned and its sequence has been determined (accession number U01030) (22a, 129). GcvA is a member of the LysR family of activator proteins and shows most similarity to the AmpR subfamily described for Citrobacter freundii and other gram-negative bacteria (86). In addition, GcvA has the ability to activate the C. freundii ampC β-lactamase gene, presumably owing to its homology with the AmpR subfamily of proteins (22a). GcvA has been partially purified and binds to two regions in a DNA fragment carrying the gcv control region (132), suggesting a direct involvement of GcvA in gcv expression.
The gcvA gene is autogenously regulated over a two- to threefold range (129). However, it is neither induced by glycine nor repressed by inosine (129), suggesting that the opposite effects of GcvA on gcv expression in the presence of glycine or inosine are mediated through the GcvA protein itself, perhaps by the binding of different cofactors to specific sites of the GcvA protein.
lrp mutations result in low noninducible levels of the GCV enzymes and gcv-lacZ fusions (45, 103). A deletion analysis showed that sequences more than 170 bp upstream of the +1 transcription initiation site are required for GcvA- and Lrp-mediated activation of the gcv promoter (103). A DNase I footprint assay demonstrated that Lrp binds to multiple sites in the gcv control region from about nucleotides –92 to –229 upstream of +1 (103), suggesting a direct involvement of Lrp in gcv expression.
The DNA sequence upstream of the gcv promoter is AT rich and has numerous A tracts (Fig. 3). Such sequences induce bending in DNA (30). Sequences from –69 to –244 cause about a 24° bend of this DNA region (L. T. Stauffer and G. V. Stauffer, unpublished data). Whether bending is required for gcv expression is unknown. In addition, how GcvA and Lrp proteins function to regulate gcv expression and whether these proteins function independently or are part of a common mechanism are unknown.
Glycyl-tRNA synthetase, encoded by glyS, has an α 2 β 2 structure, with subunit molecular weights of 33,000 (α) and 80,000 (β) (40, 87, 128). Seryl-tRNA synthetase, encoded by serS, is an α 2 dimer with a subunit molecular weight of about 50,000 (34, 44, 87). Glycyl- and seryl-tRNA synthetases show metabolic regulation, remaining approximately in balance with growth rate (58, 79). The rate of seryl-tRNA synthetase synthesis is temperature dependent, dropping from 100% to near zero as the temperature increases from 40 to 44°C (35). Also, serR encodes a putative protein that causes elevated levels of seryl-tRNA synthetase, but the mechanism is unknown (114).
The E. coli glycine transport system, encoded by cycA (also designated dagA), transports glycine, d-alanine, d-serine, and d-cycloserine (9, 127). This is the major route of glycine entry (Km of 4 μM), although other routes of entry may function at higher concentrations of amino acid (81). The system is formed constitutively (9). cycA has been cloned (28), and a detailed analysis of the transport system should be possible.
There are several transport systems for serine. One is a threonine-serine system, which is a Na+-coupled cotransport system (31). A second is the leucine, isoleucine, and valine transport system (81). A third is specific for l-serine, induced by l-leucine and coupled to H+ (32). A final threonine-serine transport system encoded by tdcC is Na+ independent and anaerobically expressed (112).
Studies from my laboratory cited in this review were supported by Public Health Service grant GM-26878 from the National Institute of General Medical Sciences.
References
1. Aronson, B. D., M. Levinthal, and R. L. Somerville. 1989. Activation of a cryptic pathway for threonine metabolism via specific IS3-mediated alteration of promoter structure in Escherichia coli. J. Bacteriol. 171:5503–5511.
2. Bachmann, B. J. 1990. Linkage map of Escherichia coli K-12, edition 8. Microbiol. Rev. 54:130–197.
3. Barak, Z., D. M. Chipman, and N. Gollop. 1987. Physiological implications of the specificity of acetohydroxy acid synthase isozymes of enteric bacteria. J. Bacteriol. 169:3750–3756.
4. Berberich, M. A., J. S. Kovach, and R. F. Goldberger. 1967. Chain initiation in a polycistronic message: sequential versus simultaneous derepression of the enzymes for histidine biosynthesis in Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 57:1857–1864.
5. Blakley, R. L. 1969. The Biochemistry of Folic Acid and Related Pteridines. Elsevier/North-Holland Publishing Co., Amsterdam.
6. Bochner, B. R., and B. N. Ames. 1982. ZTP (5-amino 4-imidazole carboxamide riboside 5'-triphosphate): a proposed alarmone for 10-formyl-tetrahydrofolate deficiency. Cell 29:929–937.
7. Byerly, K. A., M. L. Urbanowski, and G. V. Stauffer. 1991. The MetR binding site in the Salmonella typhimurium metH gene: DNA sequence constraints on activation. J. Bacteriol. 173:3547–3553.
8. Calvo, J. M., and R. G. Matthews. 1994. The leucine responsive regulatory protein, a global regulator of metabolism in Escherichia coli. Microbiol. Rev. 58:466–490.
9. Cosloy, S. D. 1973. d-Serine transport system in Escherichia coli K-12. J. Bacteriol. 114:679–684.
10. Cosloy, S. D., and E. McFall. 1970. l-Serine-sensitive mutants of Escherichia coli K-12. J. Bacteriol. 103:840–841.
11. Cowan, J. M., M. L. Urbanowski, M. Talmi, and G. V. Stauffer. 1993. Regulation of the Salmonella typhimurium metF gene by the MetR protein. J. Bacteriol. 175:5862–5866.
12. Danchin, A., and L. Dondon. 1980. Serine sensitivity of Escherichia coli K-12: partial characterization of a serine resistant mutant that is extremely sensitive to 2-ketobutyrate. Mol. Gen. Genet. 178:155–164.
13. De Felice, M., and M. Levinthal. 1977. The acetohydroxy acid synthase III isoenzyme of Escherichia coli K-12: regulation of synthesis by leucine. Biochem. Biophys. Res. Commun. 79:82–87.
14. Dempsey, W. B. 1969. 3-Phosphoserine transaminase mutants of Escherichia coli B. J. Bacteriol. 100:1114–1115.
15. Dempsey, W. B., and H. Itoh. 1970. Characterization of pyridoxine auxotrophs of Escherichia coli: serine and pdxF mutants. J. Bacteriol. 104:658–667.
16. Dev, I. K., and R. J. Harvey. 1984. Regulation of synthesis of serine hydroxymethyltransferase in chemostat cultures of Escherichia coli. J. Biol. Chem. 259:8394–8401.
17. Dev, I. K., and R. J. Harvey. 1984. Role of methionine in the regulation of the synthesis of serine hydroxymethyltransferase in Escherichia coli. J. Biol. Chem. 259:8402–8406.
18. Dubrow, R., and L. I. Pizer. 1977. Transient kinetic studies on the allosteric transition of phosphoglycerate dehydrogenase. J. Biol. Chem. 252:1527–1538.
19. Dubrow, R., and L. I. Pizer. 1977. Transient kinetic and deuterium isotope effect studies on the catalytic mechanism of phosphoglycerate dehydrogenase. J. Biol. Chem. 252:1539–1551.
20. Duerre, J. A., and R. D. Walker. 1977. Metabolism of adenosylhomocysteine, p. 43–57. In F. Salvatore, E. Borek, V. Zappia, H. G. Williams-Ashman, and F. Schlenk (ed.), The Biochemistry of Adenosylmethionine. Columbia University Press, New York.
21. Duncan, K., and J. R. Coggins. 1986. The serC-aroA operon of Escherichia coli. A mixed function operon encoding enzymes from two different amino acid biosynthetic pathways. Biochem. J. 234:49–57.
22. Ernsting, B. R., M. R. Atkinson, A. J. Ninfa, and R. G. Matthews. 1992. Characterization of the regulon controlled by the leucine-responsive regulatory protein in Escherichia coli. J. Bacteriol. 174:1109–1118.
22a. Everett, M., T. Walsh, G. Guay, and P. Bennett. 1995. GcvA, a LysR-type transcriptional regulator protein, activates expression of the cloned Citrobacter freundii ampC β-lactamase gene in Escherichia coli: cross-talk between DNA-binding proteins. Microbiology 141:419–430.
23. Folk, W. R., and P. Berg. 1970. Isolation and partial characterization of Escherichia coli mutants with altered glycyl transfer ribonucleic acid synthetases. J. Bacteriol. 102:193–203.
24. Fraser, J., and E. B. Newman. 1975. Derivation of glycine from threonine in Escherichia coli K-12 mutants. J. Bacteriol. 122:810–817.
25. Fujiwara, K., K. Okamura, and Y. Motokawa. 1979. Hydrogen carrier protein from chicken liver: purification, characterization, and role of its prosthetic group, lipoic acid, in the glycine cleavage reaction. Arch. Biochem. Biophys. 197:454–462.
26. Fujiwara, K., K. Okamura-Ikeda, and Y. Motokawa. 1984. Mechanism of the glycine cleavage reaction: further characterization of the intermediate attached to H-protein and of the reaction catalyzed by T-protein. J. Biol. Chem. 259:10664–10668.
27. Gage, D. J., and F. C. Neidhardt. 1993. Modulation of the heat shock response by one-carbon metabolism in Escherichia coli. J. Bacteriol. 175:1961–1970.
28. Ghrist, A. C., and G. V. Stauffer. 1995. The Escherichia coli glycine transport system and its role in the regulation of the glycine cleavage enzyme system. Microbiology 141:133–140.
29. Greene, R. C., and C. Radovich. 1975. Role of methionine in the regulation of serine hydroxymethyltransferase in Escherichia coli. J. Bacteriol. 124:269–278.
30. Hagerman, P. J. 1990. Sequence-directed curvature of DNA. Annu. Rev. Biochem. 59:755–781.
31. Hama, H., T. Shimamoto, M. Tsuda, and T. Tsuchiya. 1987. Properties of a Na+-coupled serine-threonine transport system in Escherichia coli. Biochim. Biophys. Acta 905:231–239.
32. Hama, H., T. Shimamoto, M. Tsuda, and T. Tsuchiya. 1988. Characterization of a novel l-serine transport system in Escherichia coli. J. Bacteriol. 170:2236–2239.
33. Hama, H., Y. Sumita, Y. Kakutagi, M. Tsuda, and T. Tsuchiya. 1990. Target of serine inhibition in Escherichia coli. Biochem. Biophys. Res. Commun. 168:1211–1216.
34. Hartlein, M., D. Madern, and R. Leberman. 1987. Cloning and characterization of the gene for Escherichia coli seryl-tRNA synthetase. Nucleic Acids Res. 15:1005–1017.
35. Hill, R. J., and W. Konigsberg. 1980. Mutation in the structural gene for seryl-transfer ribonucleic acid synthetase of Escherichia coli which affects formation of its gene product at high temperature. J. Bacteriol. 141:1163–1169.
36. Hiraga, K., and G. Kikuchi. 1980. The mitochondrial glycine cleavage system: functional association of glycine decarboxylase and aminomethyl carrier protein. J. Biol. Chem. 255:11671–11676.
37. Isenberg, S., and E. B. Newman. 1974. Studies on l-serine deaminase in Escherichia coli K-12. J. Bacteriol. 118:53–58.
38. Jerez, C., and H. Weissbach. 1980. Methylation of newly synthesized ribosomal protein L11 in a DNA-directed in vitro system. J. Biol. Chem. 255:8706–8710.
39. Jordan, P. M., and D. Shemin. 1972. δ-Aminolevulinic acid synthetase, p. 339–356. In P. D. Boyer (ed.), The Enzymes, vol. 7. Academic Press, Inc., New York.
40. Keng, T., T. A. Webster, R. T. Sauer, and P. Schimmel. 1982. Gene for Escherichia coli glycyl-tRNA synthetase has tandem subunit coding regions in the same reading frame. J. Biol. Chem. 257:12503–12508.
41. Kikuchi, G. 1973. The glycine cleavage system: composition, reaction mechanism, and physiological significance. Mol. Cell. Biochem. 1:169–187.
42. Kilstrup, M., L. M. Meng, J. Neuhard, and P. Nygaard. 1989. Genetic evidence for a repressor of synthesis of cytosine deaminase and purine biosynthesis enzymes in Escherichia coli. J. Bacteriol. 171:2124–2127.
43. Lark, C. 1979. Methylation-dependent DNA synthesis in Escherichia coli mediated by DNA polymerase I. J. Bacteriol. 137:44–50.
44. Leberman, R., M. Hartlein, and S. Cusack. 1991. Escherichia coli seryl-tRNA synthetase: the structure of a class 2 aminoacyl-tRNA synthetase. Biochim. Biophys. Acta 1089:287–298.
45. Lin, R., R. D’Ari, and E. B. Newman. 1992. λ placMu insertions in genes of the leucine regulon: extension of the regulon to genes not regulated by leucine. J. Bacteriol. 174:1948–1955.
46. Lin, R. T., R. D’Ari, and E. B. Newman. 1990. The leucine regulon of Escherichia coli K-12: a mutant in rblA alters expression of l-leucine-dependent metabolic operons. J. Bacteriol. 172:4529–4535.
46a. Lorenz, E., and G.V. Stauffer. 1995. Characterization of the MetR binding sites for the glyA gene of Escherichia coli. J. Bacteriol. 177:4113–4120.
47. Mansouri, A., J. B. Decter, and R. Silber. 1972. Studies on the regulation of one-carbon metabolism II. Repression-derepression of serine hydroxymethyltransferase by methionine in Escherichia coli 113–3. J. Biol. Chem. 247:348–352.
48. Mares, R., M. L. Urbanowski, and G. V. Stauffer. 1992. Regulation of the Salmonella typhimurium metA gene by the MetR protein and homocysteine. J. Bacteriol. 174:390–397.
49. Matthews, R. G., and F. C. Neidhardt. 1988. Abnormal induction of heat shock proteins in an Escherichia coli mutant deficient in adenosylmethionine synthetase activity. J. Bacteriol. 170:1582–1588.
50. Matthews, R. G., and F. C. Neidhardt. 1989. Elevated serine catabolism is associated with the heat shock response in Escherichia coli. J. Bacteriol. 171:2619–2625.
51. McKitrick, J. C., and L. I. Pizer. 1980. Regulation of phosphoglycerate dehydrogenase levels and effect on serine synthesis in Escherichia coli K-12. J. Bacteriol. 141:235–245.
52. Meedel, T. H., and L. I. Pizer. 1974. Regulation of one-carbon biosynthesis and utilization in Escherichia coli. J. Bacteriol. 118:905–910.
53. Miller, B. A., and E. B. Newman. 1974. Control of serine transhydroxymethylase synthesis in Escherichia coli K12. Can. J. Microbiol. 20:41–47.
54. Miller, D. A., and S. Simmonds. 1957. The metabolism of l-threonine and glycine by Escherichia coli. Proc. Natl. Acad. Sci. USA 43:195–199.
55. Motokawa, Y., and G. Kikuchi. 1974. Glycine metabolism by rat liver mitochondria. Arch. Biochem. Biophys. 164:624–633.
56. Mudd, S. H., and G. L. Cantoni. 1964. Biological transmethylation, methyl-group neogenesis and other "one-carbon" metabolic reactions dependent upon tetrahydrofolic acid, p. 1–47. In M. Florkin and E. H. Stotz (ed.), Comprehensive Biochemistry, vol. 15. Elsevier, Amsterdam.
57. Nau, F. 1976. The methylation of tRNA. Biochimie 58:629–645.
58. Neidhardt, F. C., P. L. Bloch, S. Pedersen, and S. Reeh. 1977. Chemical measurement of steady-state levels of ten aminoacyl-transfer ribonucleic acid synthetases in Escherichia coli. J. Bacteriol. 129:378–387.
59. Neuwald, A. F., D. E. Berg, and G. V. Stauffer. 1992. Mutational analysis of the Escherichia coli serB promoter region reveals transcriptional linkage to a downstream gene. Gene 120:1–9.
60. Neuwald, A. F., and G. V. Stauffer. 1985. DNA sequence and characterization of the Escherichia coli serB gene. Nucleic Acids Res. 13:7025–7039.
61. Neuwald, A. F., and G. V. Stauffer. 1989. An Escherichia coli membrane protein with a unique signal sequence. Gene 82:219–228.
62. Newman, E. B., R. D’Ari, and R. T. Lin. 1992. The leucine-Lrp regulon in E. coli: a global response in search of a raison d’etre. Cell 68:617–619.
63. Newman, E. B., V. Kapoor, and R. Potter. 1976. Role of l-threonine dehydrogenase in the catabolism of threonine and synthesis of glycine by Escherichia coli. J. Bacteriol. 126:1245–1249.
64. Newman, E. B., and B. Magasanik. 1963. The relation of serine-glycine metabolism to the formation of single-carbon units. Biochim. Biophys. Acta 78:437–448.
65. Newman, E. B., B. Miller, and V. Kapoor. 1974. Biosynthesis of single-carbon units in Escherichia coli K12. Biochim. Biophys. Acta 338:529–539.
66. Okamura-Ikeda, K., Y. Ohmura, K. Fujiwara, and Y. Motokawa. 1993. Cloning and nucleotide sequence of the gcv operon encoding the Escherichia coli glycine-cleavage system. Eur. J. Biochem. 216:539–548.
67. Pizer, L. I. 1963. The pathway and control of serine biosynthesis in Escherichia coli. J. Biol. Chem. 238:3934–3944.
68. Pizer, L. I., J. McKitrick, and T. Tosa. 1972. Characterization of a mutant of E. coli with elevated levels of seryl-tRNA synthetase. Biochem. Biophys. Res. Commun. 49:1351–1357.
69. Pizer, L. I., and M. L. Potochny. 1964. Nutritional and regulatory aspects of serine metabolism in Escherichia coli. J. Bacteriol. 88:611–619.
70. Plamann, M. D., W. D. Rapp, and G. V. Stauffer. 1983. Escherichia coli K12 mutants defective in the glycine cleavage enzyme system. Mol. Gen. Genet. 192:15–20.
71. Plamann, M. D., and G. V. Stauffer. 1983. Characterization of the Escherichia coli gene for serine hydroxymethyltransferase. Gene 22:9–18.
72. Plamann, M. D., and G. V. Stauffer. 1985. Characterization of a cis-acting regulatory mutation that maps at the distal end of the Escherichia coli glyA gene. J. Bacteriol. 161:650–654.
73. Plamann, M. D., and G. V. Stauffer. 1989. Regulation of the Escherichia coli glyA gene by the metR gene product and homocysteine. J. Bacteriol. 171:4958–4962.
74. Plamann, M. D., and G. V. Stauffer. 1990. Escherichia coli glyA mRNA decay: the role of 3' secondary structure and the effects of the pnp and rnb mutations. Mol. Gen. Genet. 220:301–306.
75. Plamann, M. D., L. T. Stauffer, M. L. Urbanowski, and G. V. Stauffer. 1983. Complete nucleotide sequence of the E. coli glyA gene. Nucleic Acids Res. 11:2065–2075.
76. Potter, R., V. Kapoor, and E. B. Newman. 1977. Role of threonine dehydrogenase in Escherichia coli threonine degradation. J. Bacteriol. 132:385–391.
77. Ravnikar, P. D., and R. L. Somerville. 1987. Genetic characterization of a highly efficient alternate pathway of serine biosynthesis in Escherichia coli. J. Bacteriol. 169:2611–2617.
78. Ravnikar, P. D., and R. L. Somerville. 1987. Structural and functional analysis of a cloned segment of Escherichia coli DNA that specifies proteins of a C4 pathway of serine biosynthesis. J. Bacteriol. 169:4716–4721.
79. Reeh, S., S. Pedersen, and F. C. Neidhardt. 1977. Transient rates of synthesis of five aminoacyl-transfer ribonucleic acid synthetases during a shift-up of Escherichia coli. J. Bacteriol. 129:702–706.
80. Rex, J. H., B. D. Aronson, and R. L. Somerville. 1991. The tdh and serA operons of Escherichia coli: mutational analysis of the regulatory elements of leucine-responsive genes. J. Bacteriol. 173:5944–5953.
81. Robbins, J. C., and D. L. Oxender. 1973. Transport systems for alanine, serine, and glycine in Escherichia coli K-12. J. Bacteriol. 116:12–18.
82. Rohlman, C. E., and R. G. Matthews. 1990. Role of purine biosynthetic intermediates in response to folate stress in Escherichia coli. J. Bacteriol. 172:7200–7210.
83. Rolfes, R. J., and H. Zalkin. 1988. Escherichia coli gene purR encoding a repressor protein for purine nucleotide synthesis. J. Biol. Chem. 263:19653–19661.
84. Rollins, C. M., and F. W. Dahlquist. 1980. Methylation of chemotaxis-specific proteins in Escherichia coli cells permeable to S-adenosylmethionine. Biochemistry 19:4627–4632.
85. Saint-Girons, I., C. Parsot, M. M. Zakin, O. Barzu, and G. N. Cohen. 1988. Methionine biosynthesis in Enterobacteriaceae: biochemical, regulatory, and evolutionary aspects. Crit. Rev. Biochem. 23:S1-S42.
86. Schell, M. A. 1993. Molecular biology of the LysR family of transcriptional regulators. Annu. Rev. Microbiol. 47:597–626.
87. Schimmel, P. 1987. Aminoacyl tRNA synthetases: general scheme of structure-function relationships in the polypeptides and recognition of transfer RNAs. Annu. Rev. Biochem. 56:125–158.
88. Schirch, L. 1984. Folates in serine and glycine metabolism, p. 399–431. In R. L. Blakley and S. J. Benkovic (ed.), Folates and Pterins: Chemistry and Biochemistry of Folates, vol. 1. Wiley-Interscience, New York.
89. Schoenlein, P. V., B. B. Roa, and M. E. Winkler. 1989. Divergent transcription of pdxB and homology between the pdxB and serA gene products in Escherichia coli K-12. J. Bacteriol. 171:6084–6092.
90. Scrimgeour, K. G., and F. M. Huennekens. 1962. Serine hydroxymethylase. Methods Enzymol. 5:838–843.
91. Silber, R., and A. Mansouri. 1971. Regulation of folate-dependent enzymes. Ann. N. Y. Acad. Sci. 186:55–69.
92. Stauffer, G. V. 1983. Regulation of serine, glycine, and one-carbon biosynthesis, p. 103–113. In K. M. Herrmann and R. L. Somerville (ed.), Amino Acids: Biosynthesis and Genetic Regulation. Addison-Wesley Publishing Co., Reading, Mass.
93. Stauffer, G. V. 1987. Biosynthesis of serine and glycine, p. 412–418. In F. C. Neidhardt, J. L. Ingraham, K. B. Low, B. Magasanik, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, vol. 1. American Society for Microbiology, Washington, D.C.
94. Stauffer, G. V., C. A. Baker, and J. E. Brenchley. 1974. Regulation of serine transhydroxymethylase activity in Salmonella typhimurium. J. Bacteriol. 120:1017–1025.
95. Stauffer, G. V., and J. E. Brenchley. 1974. Evidence for the involvement of serine transhydroxymethylase in serine and glycine interconversions in Salmonella typhimurium. Genetics 77:185–198.
96. Stauffer, G. V., and J. E. Brenchley. 1977. Influence of methionine biosynthesis on serine transhydroxymethylase regulation in Salmonella typhimurium LT2. J. Bacteriol. 129:740–749.
97. Stauffer, G. V., and J. E. Brenchley. 1978. Selection of Salmonella typhimurium mutants with altered serine transhydroxymethylase regulation. Genetics 88:221–233.
98. Stauffer, G. V., M. D. Plamann, and L. T. Stauffer. 1981. Construction and expression of hybrid plasmids containing the Escherichia coli glyA gene. Gene 14:63–72.
99. Stauffer, G. V., L. T. Stauffer, and M. D. Plamann. 1989. The Salmonella typhimurium glycine cleavage enzyme system. Mol. Gen. Genet. 220:154–156.
100. Stauffer, L. T., S. J. Fogarty, and G. V. Stauffer. 1994. Characterization of the Escherichia coli gcv operon. Gene 142:17–22.
101. Stauffer, L. T., A. Ghrist, and G. V. Stauffer. 1993. The Escherichia coli gcvT gene encoding the T-protein of the glycine cleavage enzyme system. DNA Sequence 3:339–346.
102. Stauffer, L. T., M. D. Plamann, and G. V. Stauffer. 1986. Cloning and characterization of the glycine-cleavage enzyme system of Escherichia coli. Gene 44:219–226.
103. Stauffer, L. T., and G. V. Stauffer. 1994. Characterization of the gcv control region from Escherichia coli. J. Bacteriol. 176:6159–6164.
104. Stauffer, L. T., P. S. Steiert, J. G. Steiert, and G. V. Stauffer. 1991. An Escherichia coli protein with homology to the H-protein of the glycine cleavage enzyme complex from pea and chicken liver. DNA Sequence 2:13–17.
105. Steiert, J. G., C. Kubu, and G. V. Stauffer. 1992. The PurR binding site in the glyA promoter region of Escherichia coli. FEMS Microbiol. Lett. 99:299–304.
106. Steiert, J. G., R. J. Rolfes, H. Zalkin, and G. V. Stauffer. 1990. Regulation of the Escherichia coli glyA gene by the purR gene product. J. Bacteriol. 172:3799–3803.
107. Steiert, J. G., M. L. Urbanowski, L. T. Stauffer, M. D. Plamann, and G. V. Stauffer. 1990. Nucleotide sequence of the Salmonella typhimurium glyA gene. DNA Sequence. 1:107–113.
108. Steiert, P. S., L. T. Stauffer, and G. V. Stauffer. 1990. The lpd gene product functions as the L protein in the Escherichia coli glycine cleavage enzyme system. J. Bacteriol. 172:6142–6144.
109. Stephens, P. E., H. M. Lewis, M. G. Darlison, and J. R. Guest. 1983. Nucleotide sequence of the lipoamide dehydrogenase gene of Escherichia coli K12. Eur. J. Biochem. 135:519–527.
110. Sugimoto, E., and L. I. Pizer. 1968. The mechanism of end product inhibition of serine biosynthesis. I. Purification and kinetics of phosphoglycerate dehydrogenase. J. Biol. Chem. 243:2081–2089.
111. Sugimoto, E., and L. I. Pizer. 1968. The mechanism of end product inhibition of serine biosynthesis. II. Optical studies of phosphoglycerate dehydrogenase. J. Biol. Chem. 243:2090–2098.
112. Sumantran, V. N., H. P. Schweizer, and P. Datta. 1990. A novel membrane-associated threonine permease encoded by the tdcC gene of Escherichia coli. J. Bacteriol. 172:4288–4294.
113. Taylor, R. T., H. Dickerman, and H. Weissbach. 1966. Control of one-carbon metabolism in a methionine-B12 auxotroph of Escherichia coli. Arch. Biochem. Biophys. 117:405–412.
114. Theall, G., K. B. Low, and D. Soll. 1979. Regulation of the biosynthesis of aminoacyl-tRNA synthetases and of tRNA in Escherichia coli. IV. Mutants with increased levels of leucyl- or seryl-tRNA synthetase. Mol. Gen. Genet. 169:205–211.
115. Tobey, K. L., and G. A. Grant. 1986. The nucleotide sequence of the serA gene of Escherichia coli and the amino acid sequence of the encoded protein, d-3-phosphoglycerate dehydrogenase. J. Biol. Chem. 261:12179–12183.
116. Tosa, T., and L. I. Pizer. 1971. Biochemical bases for the antimetabolite action of l-serine hydroxamate. J. Bacteriol. 106:972–982.
117. Tuan, L. R., R. D’Ari, and E. B. Newman. 1990. The leucine regulon of Escherichia coli K-12: a mutation in rblA alters expression of l-leucine-dependent metabolic operons. J. Bacteriol. 172:4529–4535.
118. Umbarger, H. E., and M. A. Umbarger. 1962. The biosynthetic pathway of serine in Salmonella typhimurium. Biochim. Biophys. Acta 62:193–195.
119. Umbarger, H. E., M. A. Umbarger, and P. M. L. Siu. 1963. Biosynthesis of serine in Escherichia coli and Salmonella typhimurium. J. Bacteriol. 85:1431–1439.
120. Urbanowski, M. L., M. D. Plamann, L. T. Stauffer, and G. V. Stauffer. 1984. Cloning and characterization of the gene for Salmonella typhimurium serine hydroxymethyltransferase. Gene 27:47–54.
121. Urbanowski, M. L., and G. V. Stauffer. 1987. Regulation of the metR gene of Salmonella typhimurium. J. Bacteriol. 169:5841–5844.
122. Urbanowski, M. L., and G. V. Stauffer. 1989. Genetic and biochemical analysis of the MetR activator-binding site in the metE metR control region of Salmonella typhimurium. J. Bacteriol. 171:5620–5629.
123. Urbanowski, M. L., L. T. Stauffer, L. S. Plamann, and G. V. Stauffer. 1987. A new methionine locus, metR, that encodes a trans-acting protein required for activation of metE and metH in Escherichia coli and Salmonella typhimurium. J. Bacteriol. 169:1391–1397.
124. Uzan, M., and A. Danchin. 1976. A rapid test for the relA mutation in E. coli. Biochem. Biophys. Res. Commun. 69:751–758.
125. Uzan, M., and A. Danchin. 1978. Correlation between the serine sensitivity and the derepressibility of the ilv genes in Escherichia coli relA – mutants. Mol. Gen. Genet. 165:21–30.
126. Vanden Boom, T. J., K. E. Reed, and J. E. Cronan, Jr. 1991. Lipoic acid metabolism in Escherichia coli: isolation of null mutants defective in lipoic acid biosynthesis, molecular cloning and characterization of the E. coli lip locus, and identification of the lipoylated protein of the glycine cleavage system. J. Bacteriol. 173:6411–6420.
127. Wargel, R. J., C. A. Shadur, and F. C. Neuhaus. 1971. Mechanism of d-cycloserine action: transport mutants for d-alanine, d-cycloserine, and glycine. J. Bacteriol. 105:1028–1035.
128. Webster, T. A., B. W. Gibson, T. Keng, K. Biemann, and P. Schimmel. 1983. Primary structures of both subunits of Escherichia coli glycyl-tRNA synthetases. J. Biol. Chem. 258:10637–10641.
129. Wilson, R. L., and G. V. Stauffer. 1994. DNA sequence and characterization of GcvA, a LysR family regulatory protein for the Escherichia coli glycine cleavage enzyme system. J. Bacteriol. 176:2862–2868.
130. Wilson, R. L., L. T. Stauffer, and G. V. Stauffer. 1993. Roles of the GcvA and PurR proteins in negative regulation of the Escherichia coli glycine cleavage enzyme system. J. Bacteriol. 175:5129–5134.
131. Wilson, R. L., P. S. Steiert, and G. V. Stauffer. 1993. Positive regulation of the Escherichia coli glycine cleavage enzyme system. J. Bacteriol. 175:902–904.
132. Wilson, R. L., M. L. Urbanowski, and G. V. Stauffer. 1995. DNA binding sites of the LysR-type regulator GcvA in the gcv and gcvA control regions of Escherichia coli. J. Bacteriol. 177:4940–4946.
Chapter30
