Molecular characterization, function and regulation of ammonium transporters (Amt) and ammonium-metabolizing enzymes (GS, NADP-GDH) in the ectomycorrhizal fungus Hebeloma cylindrosporum

Molecular Microbiology

Volumn 47, Issue 2, 2003, Pages 411-430

  Javelle, Arnaud ^a,c   Morel, Mélanie ^a   Rodríguez Pastrana, Blanca Rosa ^d   Botton, Bernard ^a   André, Bruno ^b   Marini, Anne Marie ^b   Brun, Annick ^a   Chalot, Michel ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c JOHN INNES CENTRE   (United Kingdom)

^d NONE

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; AMMONIUM TRANSPORTER; GLUTAMATE AMMONIA LIGASE; GLUTAMATE DEHYDROGENASE; GLUTAMINE; MESSENGER RNA; METHYLAMINE; NITROGEN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BINDING AFFINITY; CLONING; CONTROLLED STUDY; DOWN REGULATION; ECTOMYCORRHIZA; FUNGUS; FUNGUS GROWTH; GENE EXPRESSION; HEBELOMA CYCLINDROSPORUM; MYCELIUM; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

AGARICALES; AMINO ACID SEQUENCE; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CATION TRANSPORT PROTEINS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GLUTAMATE DEHYDROGENASE; GLUTAMATE SYNTHASE; METHYLAMINES; MOLECULAR SEQUENCE DATA; NADP; PHYLOGENY; QUATERNARY AMMONIUM COMPOUNDS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ANALYSIS, DNA;

BACTERIA (MICROORGANISMS); FUNGI; HEBELOMA CYLINDROSPORUM; MYCORRHIZAE; SACCHAROMYCES CEREVISIAE;

EID: 0037242656     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03303.x     Document Type: Article

References (99)

1. Ahmad, I., and Hellebust, J.A. (1991) Enzymology of nitrogen assimilation in mycorrhiza. Methods Microbiol 23: 181-202.
2. Alibhai, M., and Villafranca, J.J. (1994) Kinetic and mutagenic studies of the role of the active site residues Asp-50 and Glu-327 of Escherichia coli glutamine synthetase. Biochemistry 33: 682-686.
3. Avendaño, A., Deluna, A., Olivera, H., Valenzuela, L., and Gonzalez, A. (1997) GDH3 encodes a glutamate dehydrogenase isozyme, a previously unrecognized route for glutamate biosynthesis in Saccharomyces cerevisiae. J Bacteriol 179: 5594-5597.
4. Baars, J.J., Op den Camp, H.J., van Hoek, A.H., van der Drift, C., Van Griensven, L.J., Visser, J., et al. (1995) Purification and characterization of NADP-dependent glutamate dehydrogenase from the commercial mushroom Agaricus bisporus. Curr Microbiol 30: 211-217.
5. Banuett, F. (1991) Identification of genes governing filamentous growth and tumor induction by the plant pathogen Ustilago maydis. Proc Natl Acad Sci USA 88: 3922-3926.
6. Béchet, J., Grenson, M., and Wiame, J.M. (1970) Mutations affecting the repressibility of arginine biosynthetic enzymes in Saccharomyces cerevisiae. Eur J Biochem 12: 31-39.
7. Botton, B., and Chalot, M. (1991) Techniques for the studies of nitrogen metabolism in ectomycorrhiza. Methods Microbiol 23: 204-244.
8. Breiman, A., and Barash, I. (1980) Methylamine and ammonia transport in Stemphylium botryosum. J Gen Microbiol 116: 201-206.
9. Brun, A., Chalot, M., Martin, F., and Botton, B. (1992) Purification and characterization of glutamine synthetase and NADP-glutamate dehydrogenase from the ectomycorrhizal fungus Laccaria laccata. Plant Physiol 99: 938-944.
10. Cain, S.M., Matzke, E.A., and Brooker, R.J. (2000) The conserved motif in hydrophilic loop 2/3 and loop 8/9 of the lactose permease of Escherichia coli. Analysis of suppressor mutations. J Membr Biol 176: 159-168.
11. Cardoza, R.E., Moralejo, F.J., Gutierrez, S., Casqueiro, J., Fierro, F., and Martin, J.F. (1998) Characterization and nitrogen-source regulation at the transcriptional level of the gdhA gene of Aspergillus awamori encoding an NADP-dependent glutamate dehydrogenase. Curr Genet 34: 50-59.
12. Carvalho, J., Bertram, P.G., Wente, S.R., and Zheng, X.F. (2001) Phosphorylation regulates the interaction between Gln3p and the nuclear import factor Srp1p. J Biol Chem 276: 25359-25365.
13. Chalot, M., and Brun, A. (1998) Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol Rev 22: 21-44.
14. Chalot, M., Kytoviita, M.M., Brun, A., Finlay, R.D., and Söderström, B. (1995) Factors affecting amino acid uptake by the ectomycorrhizal fungus Paxillus involutus. Mycol Res 99: 1131-1138.
15. Chalot, M., Javelle, A., Blaudez, D., Lambilliote, R., Cooke, R., Sentenac, H., et al. (2002) An update on nutrient transport in ectomycorrhizas. Plant Soil 244: 165-175.
16. Coffman, J.A., Rai, R., Cunningham, T., Svetlov, V., and Cooper, T.G. (1996) Gat1p, a GATA family protein whose production is sensitive to nitrogen catabolite repression, participates in transcriptional activation of nitrogen-catabolic genes in Saccharomyces cerevisiae. Mol Cell Biol 16: 847-858.
17. Coschigano, P.W., and Magasanik, B. (1991) The URE2 gene product of Saccharomyces cerevisiae plays an important role in the cellular response to the nitrogen source and has homology to glutathione S-transferases. Mol Cell Biol 11: 822-832.
18. Coutts, G., Thomas, G., Blakey, D., and Merrick, M. (2002) Membrane sequestration of the signal transduction protein GlnK by the ammonium transporter AmtB. EMBO J 21: 536-545.
19. Daugherty, J.R., Rai, R., el Berry, H.M., and Cooper, T.G. (1993) Regulatory circuit for responses of nitrogen catabolic gene expression to the GLN3 and DAL80 proteins and nitrogen catabolite repression in Saccharomyces cerevisiae. J Bacteriol 175: 64-73.
20. Debaud, J.C., and Gay, G. (1987) In vitro fruiting under controlled conditions of the ectomycorrhizal fungus Hebeloma cylindrosporum associated with Pinus pinaster. New Phytol 105: 429-435.
21. DeLuna, A., Avendano, A., Riego, L., and Gonzalez, A. (2001) NADP-glutamate dehydrogenase isoenzymes of Saccharomyces cerevisiae. Purification, kinetic properties, and physiological roles. J Biol Chem 276: 43775-43783.
22. Dubois, E., and Grenson, M. (1979) Methylamine/ammonia uptake systems in Saccharomyces cerevisiae: multiplicity and regulation. Mol Gen Genet 175: 67-76.
23. Froeliger, E.H., and Carpenter, B.E. (1996) NUT1, a major nitrogen regulatory gene in Magnaporthe grisea, is dispensable for pathogenicity. Mol Gen Genet 251: 647-656.
24. Fu, Y.H., and Marzluf, G.A. (1987) Molecular cloning and analysis of the regulation of nit-3, the structural gene for nitrate reductase in Neurospora crassa. Proc Natl Acad Sci USA 84: 8243-8247.
25. Gimeno, C.J., Ljungdahl, P.O., Styles, C.A., and Fink, G.R. (1992) Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68: 1077-1090.
26. Haas, H., Bauer, B., Redl, B., Stoffler, G., and Marzluf, G.A. (1995) Molecular cloning and analysis of nre, the major nitrogen regulatory gene of Penicillium chrysogenum. Curr Genet 27: 150-158.
27. 14C as the substrate. J Biol Chem 245: 4241-4250.
28. von Heijne, G. (1992) Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225: 487-494.
29. Hirokawa, T., Boon-Chieng, S., and Mitaku, S. (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14: 378-379.
30. Hofmann, K., and Stoffel, W. (1992) PROFILEGRAPH: an interactive graphical tool for protein sequence analysis. Comput Appl Biosci 8: 331-337.
31. Ito, H., Fukuda, Y., Muruta, K., and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153: 163-168.
32. Jacobs, P., Jauniaux, J.C., and Grenson, M. (1980) A cis-dominant regulatory mutation linked to the argB-argC gene cluster in Saccharomyces cerevisiae. J Mol Biol 139: 691-704.
33. Jargeat, P., Gay, G., Debaud, J.C., and Marmeisse, R. (2000) Transcription of a nitrate reductase gene isolated from the symbiotic basidiomycete fungus Hebeloma cylindrosporum does not require induction by nitrate. Mol Gen Genet 263: 948-956.
34. Javelle, A., Chalot, M., Söderström, B., and Botton, B. (1999) Ammonium and methylamine transport by the ectomycorrhizal fungus Paxillus involutus and ectomycorrhizas. FEMS Microbiol Ecol 30: 355-366.
35. Javelle, A., Rodríguez-Pastrana, B.R., Jacob, C., Botton, B., Brun, A., André, B., et al. (2001) Molecular characterization of two ammonium transporters from the ectomycorrhizal fungus Hebeloma cylindrosporum. FEBS Lett 505: 393-398.
36. Javelle, A., Bruno, A., Marini, A.M., and Chalot, M. (2003) High affinity ammonium transporters could act as nitrogen sensors during mycorrhiza morphogenesis. Trends Microbiol (in press).
37. Jentschke, G., Brandes, B., Kuhn, A.J., Schröder, W.H., and Godbold, D.L. (2001) Interdependence of phosphorus, nitrogen, potassium and magnesium translocation by the ectomycorrhizal fungus Paxillus involutus. New Phytol 149: 327-338.
38. Jessen-Marshall, A.E., Paul, N.J., and Brooker, R.J. (1995) The conserved motif, GXXX(D/E)(R/K)XG[X](R/K)(R/K), in hydrophilic loop 2/3 of the lactose permease. J Biol Chem 270: 16251-16257.
39. Kersten, M.A., Muller, Y., Op den Camp, H.J., Vogels, G.D., Van Griensven, L.J., Visser, J., et al. (1997) Molecular characterization of the glnA gene encoding glutamine synthetase from the edible mushroom Agaricus bisporus. Mol Gen Genet 256: 179-186.
40. Kersten, M.A., Arninkhof, M.J., Op den Camp, H.J., Van Griensven, L.J., and van der Drift, C. (1999) Transport of amino acids and ammonium in mycelium of Agaricus bisporus. Biochim Biophys Acta 1428: 260-272.
41. Kudla, B., Caddick, M.X., Langdon, T., Martinez-Rossi, N.M., Bennett, C.F., Sibley, S., et al. (1990) The regulatory gene areA mediating nitrogen metabolite repression in Aspergillus nidulans. Mutations affecting specificity of gene activation alter a loop residue of a putative zinc finger. EMBO J 9: 1355-1364.
42. Kyte, J., and Doolitle, R.F. (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105-132.
43. Lengeler, K.B., Davidson, R.C., D'Souza, C., Harashima, T., Shen, W.C., Wang, P., et al. (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64: 746-785.
44. Liaw, S.H., Kuo, I., and Eisenberg, D. (1995) Discovery of the ammonium substrate site on glutamine synthetase, a third cation binding site. Protein Sci 4: 2358-2365.
45. Lo, H.J., Kohler, J.R., DiDomenico, B., Loebenberg, D., Cacciapuoti, A., and Fink, G.R. (1997) Nonfilamentous C. albicans mutant are avirulent. Cell 90: 939-949.
46. Lorenz, M.C., and Heitman, J. (1998) The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae. EMBO J 17: 1236-1247.
47. Lorenz, M.C., Pan, X., Harashima, T., Cardenas, M.E., Xue, Y., Hirsch, J.P., et al. (2000) The G protein-coupled receptor GPR1 is a nutrient sensor that regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Genetics 154: 609-622.
48. Lorillou, S., Botton, B., and Martin, F. (1996) Nitrogen regulates the biosynthesis of NADP glutamate dehydrogenase in the ectomycorrhizal basidiomycete Laccaria bicolor (Maire) Orton. New Phytol 132: 289-296.
49. + by the root hair plasma membrane ammonium transporter LeAMT1;1. J Biol Chem 277: 13548-13555.
50. Madhani, H.D., and Fink, G.R. (1998) The control of filamentous differentiation and virulence in fungi. Trends Cell Biol 8: 349-353.
51. Magasanik, B., and Kaiser, C.A. (2002) Nitrogen regulation in Saccharomyces cerevisiae. Gene 290: 1-18.
52. Margelis, S., D'Souza, C., Small, A.J., Hynes, M.J., Adams, T.H., and Davis, M.A. (2001) Role of glutamine synthetase in nitrogen metabolite repression in Aspergillus nidulans. J Bacteriol 183: 5826-5833.
53. Marini, A.M., and André, B. (2000)In vivo N-glycosylation of the Mep2 high-affinity ammonium transporter of Saccharomyces cerevisiae reveals an extracytosolic N-terminus. Mol Microbiol 38: 552-564.
54. Marini, A.M., Vissers, S., Urrestarazu, A., and André, B. (1994) Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J 13: 3456-3463.
55. Marini, A.M., Soussi-Boudekou, S., Vissers, S., and André, B. (1997) A family of ammonium transporters in Saccharomyces cerevisiae. Mol Cell Biol 17: 4282-4293.
56. Marini, A.M., Matassi, G., Raynal, V., André, B., Cartron, J.P., and Cherif-Zahar, B. (2000a) The human rhesus-associated RhAG protein and a kidney homologue promote ammonium transport in yeast. Nature Genet 26: 341-344.
57. Marini, A.M., Bruno, A., Frommer, W.B., and Andre, B. (2000) Cross-talk between ammonium transporters in yeast and interference by the soybean SAT1 protein. Mol Microbiol 35: 378-385.
58. Marzluf, G.A. (1997) Molecular genetics of sulfur assimilation in filamentous fungi and yeast. Annu Rev Microbiol 51: 73-96.
59. Mawhinney, T.P., Robinett, R.S., Atalay, A., and Madson, M.A. (1986) Analysis of amino acids as their tert-butyldimethylsilyl derivatives by gas-liquid chromatography and mass spectrometry. J Chromatogr 358: 231-242.
60. Medoff, G., Sacco, M., Maresca, B., Schlessinger, D., Painter, A., Kobayashi, G.S., et al. (1986) Irreversible block of the mycelia-to-yeast phase transition of Histoplasma capsulatum. Science 231: 476-479.
61. Minehart, P.L., and Magasanik, B. (1992) Sequence of the GLN1 gene of Saccharomyces cerevisiae: role of the upstream region in regulation of glutamine synthetase expression. J Bacteriol 174: 1828-1836.
62. Mitchell, A.P., and Magasanik, B. (1984) Regulation of glutamine-repressible gene products by the GLN3 function in Saccharomyces cerevisiae. Mol Cell Biol 4: 2758-2766.
63. Monahan, B.J., Fraser, J.A., Hynes, M.J., and Davis, M.A. (2002a) Isolation and characterization of two ammonium permease genes, meaA and mepA, from Aspergillus nidulans. Eukar Cell 1: 85-94.
64. Monahan, B.J., Unkles, S.E., Tsing, I.T., Kinghorn, J.R., Hynes, M.J., and Davis, M.A. (2002b) Mutation and functional analysis of the Aspergillus nidulans ammonium permease MeaA and evidence for interaction with itself and MepA. Fungal Genet Biol 36: 35-46.
65. Montanini, B., Moretto, N., Soragni, E., Percudani, R., and Ottonello, S. (2002) A high-affinity ammonium transporter from the mycorrhizal ascomycete Tuber borchii. Fungal Genet Biol 36: 22-34.
66. Mora, J. (1990) Glutamine metabolism and cycling in Neurospora crassa. Microbiol Rev 54: 293-304.
67. Moye, W.S., Amuro, N., Rao, J.K., and Zalkin, H. (1985) Nucleotide sequence of yeast GDH1 encoding nicotinamide adenine dinucleotide phosphate-dependent glutamate dehydrogenase. J Biol Chem 260: 8502-8508.
68. Ninnemann, O., Jauniaux, J.C., and Frommer, W.B. (1994) Identification of a high affinity ammonium transporter from plants. EMBO J 13: 3464-3471.
69. Pasquier, C., and Hamodrakas, S.J. (1999) An hierarchical artificial neural network system for the classification of transmembrane proteins. Protein Eng 63: 1-4.
70. Pateman, J.A., Dunn, E., Kinghorn, J.R., and Forbes, E.C. (1974) The transport of ammonium and methylammonium in wild type and mutant cells of Aspergillus nidulans. Mol Gen Genet 133: 225-236.
71. Pazdernik, N.J., Matzke, E.A., Jessen-Marshall, A.E., and Brooker, R.J. (2000) Roles of charged residues in the conserved motif, G-X-X-X-D/E-R/K-X-G-[X]-R/K-R/K, of the lactose permease of Escherichia coli. J Membr Biol 174: 31-40.
72. Persson, B., and Argos, P. (1994) Prediction of transmembrane segments in proteins utilising multiple sequence alignments. J Mol Biol 237: 182-192.
73. Plassard, C., Scheromm, P., Mousain, D., and Salsac, L. (1991) Assimilation of mineral nitrogen and ion balance in the two partners of ectomycorrhizal symbiosis. Data Hypothesis Experientia 47: 340-349.
74. Plassard, C., Bonafos, B., and Touraine, B. (2000) Differential effects of mineral and organic N sources, and of ectomycorrhizal infection by Hebeloma cylindrosporum, on growth and N utilization in Pinus pinaster. Plant Cell Environ 23: 1195-1206.
75. + uptake in roots of Arabidopsis thaliana: evidence for regulation by root glutamine levels. Plant J 19: 143-152.
76. Roon, R.J., Levy, J.S., and Larimore, F. (1974) Negative interactions between amino acid and methylamine/ammonia transport systems of Saccharomyces cerevisiae. J Biol Chem 252: 3599-3604.
77. Roon, R., Even, H.L., Dunlop, P., and Larimore, F.L. (1975) Methylamine and ammonia transport in Saccharomyces cerevisiae. J Bacteriol 122: 502-509.
78. Rowen, D.W., Esiobu, N., and Magasanik, B. (1997) Role of GATA factor Nil2p in nitrogen regulation of gene expression in Saccharomyces cerevisiae. J Bacteriol 179: 3761-3766.
79. Saier, M.H., Jr (2000) A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol Mol Biol Rev 64: 354-411.
80. Saitou, N., and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
81. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
82. +-dependent glutamate dehydrogenase (gdhA) from Agaricus bisporus. Mol General Genet 250: 339-347.
83. ter Schure, E.G., Sillje, H.H., Verkleij, A.J., Boonstra, J., and Verrips, C.T. (1995) The concentration of ammonia regulates nitrogen metabolism in Saccharomyces cerevisiae. J Bacteriol 177: 6672-6675.
84. ter Schure, E.G., Sillje, H.H., Vermeulen, E.E., Kalhorn, J.W., Verkleij, A.J., Boonstra, J., et al. (1998) Repression of nitrogen catabolic genes by ammonia and glutamine in nitrogen-limited continuous cultures of Saccharomyces cerevisiae. Microbiology 144: 1451-1462.
85. ter Schure, E.G., van Riel, N.A., and Verrips, C.T. (2000) The role of ammonia metabolism in nitrogen catabolite repression in Saccharomyces cerevisiae. FEMS Microbiol Rev 24: 67-83.
86. Slaughter, J.C., McKernan, G., and Saita, M. (1990) Intracellular asparagine pool as a factor in control of ammonium uptake by Saccharomyces cerevisiae. Mycol Res 8: 1009-1012.
87. Smith, S.E., and Read, F.A. (1997) Mycorrhizal Symbiosis. Academic Press, London.
88. Sonnhammer, E.L., von Heijne, G., and Krogh, A. (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6: 175-182.
89. Soupene, E., He, L., Yan, D., and Kustu, S. (1998) Ammonia acquisition in enteric bacteria: physiological role of the ammonium/methylammonium transport B (AmtB) protein. Proc Natl Acad Sci USA 95: 7030-7034.
90. Soupene, E., Ramirez, R.M., and Kustu, S. (2001) Evidence that fungal MEP proteins mediate diffusion of the uncharged species NH(3) across the cytoplasmic membrane. Mol Cell Biol 21: 5733-5741.
91. 3 bidirectionally. Proc Natl Acad Sci USA 99: 3926-3931.
92. Stanbrough, M., and Magasanik, B. (1996) Two transcription factors, Gln3p and Nil1p, use the same GATAAG sites to activate the expression of GAP1 of Saccharomyces cerevisiae. J Bacteriol 178: 2465-2468.
93. Stanbrough, M., Rowen, D.W., and Magasanik, B. (1995) Role of the GATA factors Gln3p and Nil1p of Saccharomyces cerevisiae in the expression of nitrogen-regulated genes. Proc Natl Acad Sci USA 92: 9450-9454.
94. Thomas, G.H., Jonathan, G.L.M., and Merrick, M. (2000) Membrane topology of the Mep/Amt family of ammonium transporters. Mol Microbiol 37: 331-344.
95. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
96. Tusnády, G.E., and Simon, I. (2001) The HMMTOP transmembrane topology prediction server. J Chem Inf Comput Sci 41: 364-368.
97. Vallorani, L., Polidori, E., Sacconi, C., Agostini, D., Pierleoni, R., Piccoli, G., et al. (2002) Biochemical and molecular characterization of NADP-glutamate dehydrogenase from the ectomycorrhizal fungus Tuber borchii. New Phytol 154: 779-790.
98. Wiame, J.M., Grenson, M., and Arst, H.N., Jr (1985) Nitrogen catabolite repression in yeasts and filamentous fungi. Adv Microb Physiol 26: 1-88.
99. Wipf, D., Benjdia, M., Tegeder, M., and Frommer, W.B. (2002) Characterization of a general amino acid permease from Hebeloma cylindrosporum. FEBS Lett 528: 119-124.