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HORT640 - Metabolic Plant Physiology
Ammonia Assimilation and Recycling
Regulation of glutamine synthetase
Bacteria and Cyanobacteria
Most bacteria (including Escherichia coli) have a single form of GS (GSI) [L-glutamate:ammonia ligase (ADP-forming), EC 126.96.36.199] encoded by glnA (see e.g. Streicher et al, 1975; Foor et al, 1975; Kustu et al, 1979; Colombo and Villafranca, 1986).
Some bacteria have a second form of GS (GSII) encoded by glnII [e.g. Rhizobium meliloti (Arcondeguy et al, 1997), Streptomyces viridochromogenes (Behrmann et al, 1990; Hillemann et al, 1993), Streptomyces coelicolor (Fink et al, 1999), and Frankia sp. (Hosted et al, 1993; Rochefort and Benson, 1990)]. Rhizobium meliloti and Rhizobium leguminosarum have a third GS (GSIII) encoded by glnT (Espin et al, 1990; Shatters et al, 1993). Pseudanabaena sp. strain PCC 6903 is a cyanobacterium that lacks the typical prokaryotic glutamine synthetase type I encoded by the glnA gene (Crespo et al, 1998). Glutamine synthetase type III, is the only glutamine synthetase activity present in this cyanobacterium, and is encoded by glnN (Crespo et al, 1998).
GSI is subject to cumulative feedback inhibition by end-products of glutamine metabolism, ADP and AMP and other nucleotides. Glycine, alanine, and serine appear to inhibit the fully unadenylylated Salmonella typhimurium GS [with Mn2+ ions bound] by competing with the substrate glutamate for the active site (Liaw et al, 1993). Nucleotides bind at the same site; the cofactor ATP binding site of the fully unadenylylated Salmonella typhimurium GS-Mn2+ (Liaw et al, 1994). GSIII of Rhizobium sp. is inhibited by ADP and pyrophosphate but not by various nitrogen-containing metabolites that inhibit other GS enzymes (Shatters et al, 1993).
In many bacteria, GSI is finely regulated by reversible inactivation involving a glutamine-dependent covalent attachment of an adenylyl group to a tyrosyl residue (Tyr-397) of each of the 12 subunits, catalyzed by an adenylyltransferase (AT) (EC 188.8.131.52) (Berlett et al, 1998). AT catalyzes both the adenylylation and deadenylylation of glutamine synthetase in Escherichia coli (Caban and Ginsburg, 1976). The adenylyltransferase is also known as ATase [or glutamine synthetase adenylyltransferase/removase], and is encoded by glnE (Forchhammer et al, 1999).
glnE mutants show a large growth defect specifically upon shift from a nitrogen-limited growth medium to medium containing excess ammonium (Kustu et al, 1984). The growth defect appears to be due to very high catalytic activity of GS after shift, which lowers the intracellular glutamate pool to approximately 10% that under preshift conditions (Kustu et al, 1984). The glnE strains have normal ATP pools after shift but they synthesize large amounts of glutamine and excrete glutamine into the medium. The major function for adenylylation of bacterial GS is to protect the cellular glutamate pool upon shift to ammonium-excess conditions and thereby to allow rapid growth (Kustu et al, 1984). The glutamine/2-oxoglutarate ratio is critical in this control of GS.
GS can exist in various degrees of adenylylation. Because Escherichia coli GS is composed of 12 identical subunits arranged in two superimposed hexagonal arrays, partially adenylylated GS is a mixture of hybrid molecules containing different numbers (from 0 to 12) and distributions of adenylylated subunits (Chung and Rhee, 1984). The catalytic activity of GS is inversely proportional to the average number of covalently bound adenylyl groups per molecule. The adenylylated GS has a lower catalytic activity, an absolute requirement for manganese as the divalent cation, and is considerably more susceptible to feedback inhibition than the unadenylylated enzyme. The fraction of subunits that are adenylylated is determined by the concentration of over 40 metabolites (Stadtman et al, 1980).
The nitration of Tyr-397 or of the nearby Tyr-326 by peroxynitrite can convert the unadenylylated enzyme to a form exhibiting regulatory characteristics similar to the form obtained by adenylylation (Berlett et al, 1998).
The native AT is a single polypeptide chain of ~115,000 molecular weight. The enzyme is activated by ATP, L-glutamine, and the PII regulatory protein and is inhibited by 2-oxoglutarate [an activator of deadenylylation] (Caban and Ginsburg, 1976).
As noted above, deadenylylation is catalyzed by the same enzyme as involved in adenylylation. Regulation as to which reaction the adenylyltransferase catalyzes is determined by a regulatory protein, PII, which can exist in 2 forms; a form which stimulates the adenylylation of GS (PII), and a form which has a uridylyl group covalently bound to the protein (PII-UMP) and which stimulates deadenylylation of GS. PII is encoded by glnB. The interconversion of the two forms of PII is catalyzed by a uridylyltransferase (UT)/uridylyl removing (UR) enzyme, encoded by glnD, which acts as the primary nitrogen sensor in the nitrogen regulation (Ntr) system [to be discussed below].
The deadenylylation of GS requires UTP, ATP and 2-oxoglutarate and Mg2+ or Mn2+ and is inhibited by glutamine. Adenylylation of GS is stimulated by glutamine and inhibited by 2-oxoglutarate. In a reconstituted system containing GS, ATase, PII and UTase/UR, the adenylylation state of GS was regulated reciprocally by 2-oxoglutarate and glutamine (Jiang et al, 1998). The only sensors of 2-oxoglutarate appear to be PII and PII-UMP (Jiang et al, 1998). At physiological conditions, the main role of 2-oxoglutarate in bringing about the deadenylylation of GS is to inhibit GS adenylylation, due to the allosteric regulation of PII activity (Jiang et al, 1998). Glutamine acts as an allosteric regulator of both ATase and UTase/UR (Jiang et al, 1998).
The adenylytransferase has separate interaction sites for L-glutamine and the regulatory PII protein (Caban and Ginsburg, 1976). The 945 amino acid residue AT has been truncated to produce two polypeptides corresponding to amino acids 1-423 (AT-N) and 425-945 (AT-C) (Jaggi et al, 1997). AT-N carries the deadenylylation activity and AT-C carries the adenylylation activity (Jaggi et al, 1997). Glutamine activates the adenylylation reaction of the AT-C domain, whereas 2-oxooglutarate activates the deadenylylation reaction catalyzed by the AT-N domain (Jaggi et al, 1997). The deadenylylation activity of AT-N depends on PII-UMP and is inhibited by PII. The adenylylation activity of AT-C is independent of PII (or PII-UMP), whereas in the intact enzyme PII is required for this activity (Jaggi et al, 1997).
GSI is regulated by repression/derepression of its structural gene, glnA. Nitrogen control in Salmonella typhimurium is not limited to GS but affects, in addition, transport systems for histidine, glutamine, lysine-arginine-ornithine, and glutamate-aspartate. Synthesis of both GS and transport proteins is elevated by limitation of nitrogen in the growth medium (Kustu et al, 1979). A regulatory gene, "glnR", was initially proposed to be responsible for this regulation (Kustu et al, 1979). It was subsequently found that the nitrogen regulatory locus "glnR" of Escherichia coli and Salmonella typhimurium is composed of two cistrons, named ntrB = glnL and ntrC = glnG (nitrogen regulation B and C) (McFarland et al, 1981; Atkinson and Ninfa, 1998). The ntrB (glnL) gene encodes the kinase/phosphatase NRII (NtrB) (Atkinson and Ninfa, 1998). The ntrC (glnG) gene encodes the transcriptional activator NRI (NtrC) (Atkinson and Ninfa, 1998). Mutations in ntrB and ntrC were selected as suppressors of glnF (renamed ntrA) (McFarland et al, 1981). [The product of the glnF (rpoN) gene is sigma 60 (Ninfa and Magasanik, 1986), and is proposed to be a positive regulatory factor required for synthesis of GS (Garcia et al, 1977)].
E. coli has a second PII-like protein, GlnK, encoded by glnK.
It is now known that both PII (the glnB product) and GlnK (the glnK product) act through the kinase/phosphatase nitrogen regulator NRII (NtrB) to reduce transcription initiation from Ntr promoters, apparently by regulating the phosphorylation state of the transcriptional activator NRI-P (NtrC-P) (Atkinson and Ninfa, 1998; 1999). Both PII and GlnK are potent activators of the phosphatase activity of NRII (Atkinson and Ninfa, 1999). NRI-P activates transcription from nitrogen-regulated promoters; the role of NRII is to control the formation and breakdown of NRI-P in response to cellular signals of nitrogen availability (Ninfa and Magasanik, 1986).
The removal of uridylyl groups from the PII protein, catalyzed by the UTase/UR protein in the presence of glutamine, results in the stimulation of NRI-P dephosphorylation (Atkinson et al, 1994). In contrast, the uridylylated form of the PII protein has no discernible effect on NRI phosphorylation (Atkinson et al, 1994).
Both GlnK and PII act through adenylyltransferase (ATase, the glnE product) to regulate the adenylylation state of GS. The activity of both GlnK and PII is regulated by the signal-transducing uridylyltransferase/uridylyl-removing enzyme (UTase/UR, glnD product) (Atkinson and Ninfa, 1998). However, while both GlnK and PII were readily uridylylated by the uridylyltransferase activity of UTase/UR, only PII-UMP was effectively deuridylylated by the UR activity of UTase/UR (Atkinson and Ninfa, 1999).
PII-like signalling molecules are trimeric proteins composed of 12-13 kDa polypeptides. GlnK and PII (GlnB) of E. coli form heterotrimers with each other (Forchhammer et al, 1999; van Heeswijk et al, 2000).
Thus, the PII paralogs are Escherichia coli's cognate transducers of the nitrogen signal to the NRII (NtrB)/NRI (NtrC) two-component system and to adenylyltransferase (van Heeswijk et al, 2000). Through these two routes, PII paralogs regulate both amount and activity of glutamine synthetase (van Heeswijk et al, 2000).
Evidence for adenylylation of GS have been reported in Klebsiella aerogenes (Foor et al, 1975), Corynebacterium glutamicum (Jakoby et al, 1999), Pseudomonas aeruginosa (Janssen et al, 1980; 1982), Photobacterium phosphoreum (Kimura et al, 1986), Mycobacterium smegmatis (Kimura et al, 1986), Rhodospirillum rubrum (Johansson and Nordlund, 1999) and Streptomyces coelicolor (Fink et al, 1999).
Bacillus subtilis GS is NOT regulated by adenylylation (Orr et al, 1981).
In Bacillus subtilis nitrogen metabolism genes are regulated by the availability of rapidly metabolizable nitrogen sources, but not by the two-component Ntr regulatory system found in enteric bacteria (Fisher, 1999). Three regulatory proteins (GlnR, TnrA and CodY) independently control the expression of gene products involved in nitrogen metabolism in response to nutrient availability (Fisher, 1999). The TnrA protein is active only during nitrogen limitation, whereas GlnR-dependent repression occurs in cells growing with excess nitrogen. Although the nitrogen signal regulating the activity of the GlnR and TnrA proteins is not known, the wild-type glutamine synthetase protein is required for the transduction of this signal to the GlnR and TnrA proteins (Fisher, 1999). A third regulatory protein, CodY, controls the expression of several genes involved in nitrogen metabolism, competence and acetate metabolism in response to growth rate (Fisher, 1999).
GlnR, encoded by glnR, is a DNA binding protein directly responsible for regulating the expression of the glutamine synthetase operon (glnRA) in Bacillus subtilis (Gutowski and Schreier, 1992). GlnR is a dimer with a molecular weight of
approximately 30,000, and subunit molecular weight of 15,000. GlnR protein binds specifically to the promoter region of the glnRA operon of Bacillus subtilis and B. cereus (Nakano and Kimura, 1991). The binding of the GlnR protein to the glnRA was enhanced by the presence of GS, the product of glnA, of B. cereus or B. subtilis (Nakano and Kimura, 1991). Regulation of glnA expression may thus require both GlnR protein and GS in Bacillus (Nakano and Kimura, 1991).
TnrA is a transcription factor required for global nitrogen regulation in Bacillus subtilis (Wray et al, 1996). The tnrA mutant is impaired in its ability to utilize allantoin, gamma-aminobutyrate, isoleucine, nitrate, urea, and valine as nitrogen sources (Wray et al, 1996). During nitrogen-limited growth, transcription of the nrgAB, nasB, gabP, and ure genes is significantly reduced in the tnrA mutant compared with the levels seen in wild-type cells (Wray et al, 1996). In contrast, the level of glnRA expression is 4-fold higher (Wray et al, 1996).
In the Rhizobiaceae, glnII is regulated by the NtrC protein (encoded by ntrC) (Patriarca et al, 1994). PII (encoded by glnB) is required for expression of the ntrC-dependent gene glnII and for adenylylation of GSI (encoded by glnA) in Rhizobium meliloti (Arcondeguy et al, 1997).
Biochemical and genetic evidence suggests that cyanobacteria lack adenylyltransferase (Emond et al, 1979; Orr et al, 1981; Fisher et al, 1981; Brown et al, 1994). Although cyanobacteria lack adenylylation regulation of GS, and may have secondarily lost it (Brown et al, 1994), they contain PII and uridylyltranferase paralogs (see e.g. Forchhammer et al, 1999).
Heterologous expression of a cyanobacterial glnB gene in Escherichia coli leads to an inactivation of E. coli's own PII signalling system; this effect is caused by the formation of functionally inactive heterotrimers between the cyanobacterial glnB gene product and the E. coli PII paralogs GlnB and GlnK (Forchhammer and Hedler, 1997; Forchhammer et al, 1999).
Cyanobacterial GS is controlled by a different mechanism that involves the interaction of two inhibitory polypeptides with the enzyme. Both inactivating factors (IFs), named IF7 and IF17, are required in vivo for complete GS inactivation (Garcia-Dominguez et al, 1999). The gifA and gifB genes encode the inhibitors of glutamine synthetase type I from Synechocystis sp. PCC 6803. The transcription factor NtcA represses transcription of gifA and gifB (Garcia-Dominguez et al, 2000). Thus, NtcA plays a central role in GS regulation in cyanobacteria, stimulating transcription of the glnA gene (GS structural gene) and suppressing transcription of the GS inactivating factor genes gifA and gifB (Garcia-Dominguez et al, 2000).
In Pseudanabaena sp. strain PCC 6903 [a cyanobacterium that lacks the typical prokaryotic glutamine synthetase type I encoded by the glnA gene], glutamine synthetase type III, encoded by glnN, is also subject to NtcA control (Crespo et al, 1998).
Arcondeguy T, Huez I, Tillard P, Gangneux C, de Billy F, Gojon A, Truchet G, Kahn D 1997 The Rhizobium meliloti PII protein, which controls bacterial nitrogen metabolism, affects alfalfa nodule development. Genes Dev. 11: 1194-1206.
Atkinson MR, Kamberov ES, Weiss RL, Ninfa AJ 1994 Reversible uridylylation of the Escherichia coli PII signal transduction protein regulates its ability to stimulate the dephosphorylation of the transcription factor nitrogen regulator I (NRI or NtrC). J. Biol. Chem. 269: 28288-28293.
Atkinson MR, Ninfa AJ 1998 Role of the GlnK signal transduction protein in the regulation of nitrogen assimilation in Escherichia coli. Mol. Microbiol. 29: 431-447.
Atkinson MR, Ninfa AJ 1999 Characterization of the GlnK protein of Escherichia coli. Mol. Microbiol. 32: 301-313.
Behrmann I, Hillemann D, Puhler A, Strauch E, Wohlleben W 1990 Overexpression of a Streptomyces viridochromogenes gene (glnII) encoding a glutamine synthetase similar to those of eucaryotes confers resistance against the antibiotic phosphinothricyl-alanyl-alanine. J. Bacteriol. 172: 5326-5334.
Berlett BS, Levine RL, Stadtman ER 1998 Carbon dioxide stimulates peroxynitrite-mediated nitration of tyrosine residues and inhibits oxidation of methionine residues of glutamine synthetase: both modifications mimic effects of adenylylation. Proc. Natl. Acad. Sci. U.S.A. 95: 2784-2789.
Brown JR, Masuchi Y, Robb FT, Doolittle WF 1994 Evolutionary relationships of bacterial and archaeal glutamine synthetase genes. J. Mol. Evol. 38: 566-576.
Caban CE, Ginsburg A 1976 Glutamine synthetase adenylyltransferase from Escherichia coli: purification and physical and chemical properties. Biochemistry 15: 1569-1580.
Chung HK, Rhee SG 1984 Separation of glutamine synthetase species with different states of adenylylation by chromatography on monoclonal anti-AMP antibody affinity columns. Proc. Natl. Acad. Sci. U.S.A. 81: 4677-4681.
Colombo G, Villafranca JJ 1986 Amino acid sequence of Escherichia coli glutamine synthetase deduced from the DNA nucleotide sequence. J. Biol. Chem. 261: 10587-10591.
Crespo JL, Garcia-Dominguez M, Florencio FJ 1998 Nitrogen control of the glnN gene that codes for GS type III, the only glutamine synthetase in the cyanobacterium Pseudanabaena sp. PCC 6903. Mol. Microbiol. 30: 1101-1112.
Emond D, Rondeau N, Cedergren RJ 1979 Distinctive properties of glutamine synthetase from the cyanobacterium Anacystis nidulans. Can. J. Biochem. 57: 843-851.
Espin G, Moreno S, Wild M, Meza R, Iaccarino M 1990 A previously unrecognized glutamine synthetase expressed in Klebsiella pneumoniae from the glnT locus of Rhizobium leguminosarum. Mol. Gen. Genet. 223: 513-516.
Fink D, Falke D, Wohlleben W, Engels A 1999 Nitrogen metabolism in Streptomyces coelicolor A3(2): modification of glutamine synthetase I by an adenylyltransferase. Microbiology 145: 2313-2322.
Fisher SH 1999 Regulation of nitrogen metabolism in Bacillus subtilis: vive la difference! Mol. Microbiol. 32: 223-232.
Fisher R, Tuli R, Haselkorn R 1981 A cloned cyanobacterial gene for glutamine synthetase functions in Escherichia coli, but the enzyme is not adenylylated. Proc. Natl. Acad. Sci. U.S.A. 78: 3393-3397.
Foor F, Janssen KA, Magasanik B 1975 Regulation of synthesis of glutamine synthetase by adenylylated glutamine synthetase. Proc. Natl. Acad. Sci. U.S.A. 72: 4844-4848.
Forchhammer K, Hedler A 1997 Phosphoprotein PII from cyanobacteria--analysis of functional conservation with the PII signal-transduction protein from Escherichia coli. Eur. J. Biochem. 244: 869-875.
Forchhammer K, Hedler A, Strobel H, Weiss V 1999 Heterotrimerization of PII-like signalling proteins: implications for PII-mediated signal transduction systems. Mol. Microbiol. 33: 338-349.
Garcia E, Bancroft S, Rhee SG, Kustu S 1977 The product of a newly identified gene, glnF, is required for synthesis of glutamine synthetase in Salmonella. Proc. Natl. Acad. Sci. U.S.A. 74: 1662-1666.
Garcia-Dominguez M, Reyes JC, Florencio FJ 1999 Glutamine synthetase inactivation by protein-protein interaction. Proc. Natl. Acad. Sci. U.S.A. 96: 7161-7166.
Garcia-Dominguez M, Reyes JC, Florencio FJ 2000 NtcA represses transcription of gifA and gifB, genes that encode inhibitors of glutamine synthetase type I from Synechocystis sp. PCC 6803. Mol. Microbiol. 35: 1192-1201
Gutowski JC, Schreier HJ 1992 Interaction of the Bacillus subtilis glnRA repressor with operator and promoter sequences in vivo. J. Bacteriol. 174: 671-681.
Hillemann D, Dammann T, Hillemann A, Wohlleben W 1993 Genetic and biochemical characterization of the two glutamine synthetases GSI and GSII of the phosphinothricyl-alanyl-alanine producer, Streptomyces viridochromogenes Tu494. J. Gen. Microbiol. 139: 1773-1783.
Hosted TJ, Rochefort DA, Benson DR 1993 Close linkage of genes encoding glutamine synthetases I and II in Frankia alni CpI1. J. Bacteriol. 175: 3679-3684.
Jaggi R, van Heeswijk WC, Westerhoff HV, Ollis DL, Vasudevan SG 1997 The two opposing activities of adenylyl transferase reside in distinct homologous domains, with intramolecular signal transduction. EMBO J. 16: 5562-5571.
Jakoby M, Kramer R, Burkovski A 1999 Nitrogen regulation in Corynebacterium glutamicum: isolation of genes involved and biochemical characterization of corresponding proteins. FEMS Microbiol. Lett. 173: 303-310.
Janssen DB, Habets WJ, Marugg JT, Van Der Drift C 1982 Nitrogen control in Pseudomonas aeruginosa: mutants affected in the synthesis of glutamine synthetase, urease, and NADP-dependent glutamate dehydrogenase. J. Bacteriol. 151: 22-28.
Janssen DB, op den Camp HJ, Leenen PJ, van der Drift C 1980 The enzymes of the ammonia assimilation in Pseudomonas aeruginosa. Arch. Microbiol. 124: 197-203.
Jiang P, Peliska JA, Ninfa AJ 1998 The regulation of Escherichia coli glutamine synthetase revisited: role of 2-ketoglutarate in the regulation of glutamine synthetase adenylylation state. Biochemistry 37: 12802-12810.
Johansson M, Nordlund S 1999 Purification of P(II) and P(II)-UMP and in vitro studies of regulation of glutamine synthetase in Rhodospirillum rubrum. J. Bacteriol. 181: 6524-6529.
Kimura K, Matsuoka K, Kobayashi H 1986 Regulation and properties of the glutamine synthetase purified from Photobacterium phosphoreum. J. Biochem. (Tokyo) 99: 111-117.
Kustu S, Hirschman J, Burton D, Jelesko J, Meeks JC 1984 Covalent modification of bacterial glutamine synthetase: physiological significance. Mol. Gen. Genet. 197: 309-317.
Kustu SG, McFarland NC, Hui SP, Esmon B, Ames GF 1979 Nitrogen control of Salmonella typhimurium: co-regulation of synthesis of glutamine synthetase and amino acid transport systems. J. Bacteriol. 138: 218-234.
Liaw SH, Jun G, Eisenberg D 1994 Interactions of nucleotides with fully unadenylylated glutamine synthetase from Salmonella typhimurium. Biochemistry 33: 11184-11188.
Liaw SH, Pan C, Eisenberg D 1993 Feedback inhibition of fully unadenylylated glutamine synthetase from Salmonella typhimurium by glycine, alanine, and serine. Proc. Natl. Acad. Sci. U.S.A. 90: 4996-5000.
McFarland N, McCarter L, Artz S, Kustu S 1981 Nitrogen regulatory locus "glnR" of enteric bacteria is composed of cistrons ntrB and ntrC: identification of their protein products. Proc. Natl. Acad. Sci. U.S.A. 78: 2135-2139.
Nakano Y, Kimura K 1991 Purification and characterization of a repressor for the Bacillus cereus glnRA operon. J. Biochem. (Tokyo) 109: 223-228.
Ninfa AJ, Magasanik B 1986 Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 83: 5909-5913.
Orr J, Keefer LM, Keim P, Nguyen TD, Wellems T, Heinrikson RL, Haselkorn R 1981 Purification, physical characterization, and NH2-terminal sequence of glutamine synthetase from the cyanobacterium Anabaena 7120. J. Biol. Chem. 256: 13091-13098.
Rochefort DA, Benson DR 1990 Molecular cloning, sequencing, and expression of the glutamine synthetase II (glnII) gene from the actinomycete root nodule symbiont Frankia sp. strain CpI1. J. Bacteriol. 172: 5335-5342.
Shatters RG, Liu Y, Kahn ML 1993 Isolation and characterization of a novel glutamine synthetase from Rhizobium meliloti. J. Biol. Chem. 268: 469-475.
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