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Antonie van Leeuwenhoek

, Volume 65, Issue 3, pp 169–177 | Cite as

Nitrogen regulation in fungi

  • Mark X. Caddick
  • David Peters
  • Adam Platt
Article

Abstract

Nitrogen regulation has been extensively studied in fungi revealing a complex array of interacting regulatory genes. The general characterisation of the systems inAspergillus nidulans andNeurospora crassa shall be briefly described, but much of this paper will concentrate specifically on the recent molecular characterisation ofareA, the principle regulatory gene fromA. nidulans which mediates nitrogen metabolite repression. Three areas shall be explored in detail, firstly the DNA binding domain, which has been characterised extensively by both molecular and genetic analysis. Secondly we shall report recent analysis which has revealed the presence of related DNA binding activities inA. nidulans. Finally we shall discuss the mechanism by which the nitrogen state of the cell is monitored by theareA product, in particular localisation of the domain within theareA product which mediates the regulatory response within the protein.

Key words

areA Aspergillus nidulans gata-1 nit-2 nitrogen metabolite repression Neurospora crassa 

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References

  1. Arceci RJ, King AAJ, Simon MC, Orkin SJ & Wilson DB (1993). Mouse GATA-4: A retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol. Cell. Biol. 13(4): 2235–2246PubMedGoogle Scholar
  2. Arst HN Jr (1990) Wide domain regulation of gene expression inAspergillus nidulans with specific attention to the role of themeaB gene. In: Heslot H, Davies J, Florent J, Bobichon L, Durand G & Penasse L (Eds) Proceedings of the 6th International Symposium on Genetics of Industrial Micro-organisms (GIM90), Vol II (pp 555–566). Society Francaise de Microbiologie, ParisGoogle Scholar
  3. Arst HN Jr & Bailey CR (1977) The regulation of carbon metabolism inAspergillus nidulans. In: Smith JE & Pateman JA (Eds) Genetics and Physiology ofAspergillus (pp 131–146). Academic Press, New YorkGoogle Scholar
  4. Arst HN Jr & Cove DJ (1973) Nitrogen metabolite repression inAspergillus nidulans. Mol. Gen. Genet. 126: 111–142PubMedGoogle Scholar
  5. Arst HN Jr & Scazzocchio C (1975) Initiator constitutive mutation with an ‘up-promoter’ effect inAspergillus nidulans. Nature (London) 254: 31–34PubMedGoogle Scholar
  6. Arst HN Jr & Scazzocchio C (1985) Formal genetics and molecular biology of the control of gene expression inAspergillus nidulans. In: Bennet JW & Lasure LL (Eds) Gene Manipulations in Fungi (pp 309–343). Academic Press, New YorkGoogle Scholar
  7. Arst HN Jr, Kudla B, Martinez-Rossi N, Caddick MX, Sibley S & Davies RW (1989)Aspergillus and mouse share a new class of ‘zinc finger’ protein. Trends in Genetics 5: 291PubMedGoogle Scholar
  8. Arst HN Jr, Tollervey D & Caddick MX (1989) A translocation associated, loss-of-function mutation in the nitrogen metabolite repression regulatory gene ofAspergillus nidulans can revert intracistronicially. Mol. Gen. Genet. 215: 364–367PubMedGoogle Scholar
  9. Bailey C & Arst HN Jr (1975) Carbon catabolite repression inAspergillus nidulans. Eur. J. Biochem. 51: 573–577PubMedGoogle Scholar
  10. Bysani N, Daugherty JR & Cooper TG, (1991). Saturation mutagenesis of theUAS NTR (GATAA) responsible for nitrogen catbaolite repression-sensitive transcriptional activation of the allantoin pathway genes inSaccharomyces cerevisiae. J. Bacteriol. 173: 4977–4982PubMedGoogle Scholar
  11. Caddick MX (in press). Nitrogen metabolite repression. In: Kinghorn JR & Martinelli SD (Eds) Genetics and Physiology ofAspergillus, Elsevier, AmsterdamGoogle Scholar
  12. Caddick MX & Arst HN Jr (1990) Nitrogen regulation inAspergillus: Are two fingers better than one? Gene 99: 123–127Google Scholar
  13. Caddick MX & Turner AS (1993) The control of gene expression in filamentous fungi. In: Broda PMA, Oliver SG, & Sims PFG (Eds) The Eukaryotic Genome Organisation and Regulation (pp 241–273). Cambridge University Press, New YorkGoogle Scholar
  14. Caddick MX, Brownlee AG & Arst HN Jr (1986) Regulation of gene expression by pH of the growth mediums inAspergillus nidulans. Mol. Gen. Genet. 203: 346–353PubMedGoogle Scholar
  15. Chiba T, Ikawa Y & Todokoro T (1991) GATA-1 transactivates erythropoietin receptor gene, and erythropoietin receptor-mediated signals enhance GATA-1 gene expression. Nucleic Acids Res. 19(14): 3843–3848PubMedGoogle Scholar
  16. Cooper TG, Ferguson, D, Rai R & Bysani N (1990) TheGLN3 gene product is required for transcriptional activation of allantoin system gene expression inSaccheromyces serevisiae. J. Bacteriol. 172: 1014–1018PubMedGoogle Scholar
  17. Cove DJ (1979) Genetic studies of nitrate assimilation inAspergillus nidulans. Biol. Rev. Cambr. Philos. Soc. 54: 291–327Google Scholar
  18. Crawford NM & Arst HN Jr (1993) The Molecular genetics of nitrate assimilation in fungi and plants. Ann. Rev. Genet. 27: 115–146PubMedGoogle Scholar
  19. Cunningham TS & Cooper TG (1991) Expression of the DAL80 gene whose product is homologous to the GATA factors and is a negative regulator of multiple catabolic genes inSaccharomyces cerevesiae, is sensitive to nitrogen catabolite repression. Mol. Cell. Biol. 11: 6205–6215PubMedGoogle Scholar
  20. Daniel-Vedele F & Caboche M (1993) A tobacco cDNA clone encoding a GATA-1 zinc-finger protein homologous to regulators of nitrogen metabolism in fungi. Mol. Gen. Genet. 240: 365–373PubMedGoogle Scholar
  21. Daugherty JR, Rai R, El Berry HM & Cooper TG (1993) Regulatory circuit for responses of nitrogen catabolic gene expression to the GLN3 and DAL80 proteins and nitrogen catabolite repression inSaccharomyces cerivisiae. J. Bacteriol 175: 64–73PubMedGoogle Scholar
  22. Davis MA & Hynes MJ (1987) Complementation ofareA regulatory gene mutations ofAspergillus nidulans by the heterologous regulatory genenit-2 ofNeurospora crassa. Proc. Natl. Acad. Sci. USA 84: 3753–3757PubMedGoogle Scholar
  23. Dorfman DM, Wilson DB, Bruns GAP & Orkin SH (1992) Human transcription tactor GATA-2. J. Biol. Chem. 267: 1279–1285PubMedGoogle Scholar
  24. Drainas C, Kinghorn JR & Pateman JA (1977) Aspartic hydroxamate resistance and asparaginase regulation in the fungusAspergillus nidulans. J. Gen. Microbiol. 98: 493–501Google Scholar
  25. Dunn-Coleman NS, Tomsett AB & Garrett RH (1980) The regulation of nitrate assimilation inNeurospora crassa: Biochemical analysis of thenmr-1 mutants. Mol. Gen. Genet. 182: 234–239Google Scholar
  26. Evans T & Felsenfeld G (1989) The erythroid-specific transcription factor eryf-1: A new finger protein. Cell 5: 877–885Google Scholar
  27. Fu Y-H & Marzluf GA (1990a).nit-2, the major nitrogen regulatory gene ofNeurospora crassa, encodes a protein with a putative zinc finger DNA-binding domain. Mol. Cell. Biol. 10: 1056–1065PubMedGoogle Scholar
  28. Fu Y-H & Marzluf GA (1990b) nit-2 the major positive-acting nitrogen regulatory gene ofNeurospora crassa, encodes a sequence-specific DNA-binding protein. Proc. Natl. Acad. Sci. USA 87: 5331–5335PubMedGoogle Scholar
  29. Fu Y-H, Young JL & Marzluf GA (1988) Molecular cloning and characterization of a negative-acting nitrogen regulatory gene ofNeurospora crassa. Mol. Gen. Genet. 214: 120–128Google Scholar
  30. Gussin GN, Ronson CW & Ausbel FM (1986) Regulation of nitrogen fixation. Ann. Rev. Genet. 20: 567–591PubMedGoogle Scholar
  31. Ho I-C, Vorhees P, Marin N, Oakley BK, Tsai S-F, Orkin SH & Leiden JM (1991) Human GATA-3: A lineage restricted transcription factor that regulates the expression of the T cell receptor gene. EMBO J. 10: 1809–1816PubMedGoogle Scholar
  32. Hunter T & Karin M (1992) The regulation of transcription by phosphorylation. Cell 70: 375–387PubMedGoogle Scholar
  33. Hynes MJ (1975) Studies on the role of theareA gene in the regulation of nitrogen catabolism inAspergillus nidulans. Austr. J. Biol. Sci. 28: 301–313Google Scholar
  34. Joulin V, Bories D, Eleouet J-F, Labastie M-C, Chretien S, Mattei M-G & Romeo PH (1991). A T-cell specific TCR δ DNA-binding protein is a member of the human GATA-binding family. EMBO J. 10: 1809–1816PubMedGoogle Scholar
  35. Katz ME & Hynes MJ (1989) Characterization of theamdR-controlledlamA andlamB genes ofAspergillus nidulans. Genetics 122: 331–339PubMedGoogle Scholar
  36. Ko LJ & Engel JD (1993) DNA-binding specificity of the GATA transcription factor family. Mol. Cell. Biol. 13(7): 4011–4022PubMedGoogle Scholar
  37. Kudla B, Caddick MX, Langdon T, Martinez-Rossi NM, Bennett CF, Sibley S, Davies RW & Arst HN Jr (1990) The regulatory geneareA mediating nitrogen metabolite repression inAspergillus nidulans. Mutations affecting specificity of gene activation alter a loop residue of a putative zinc finger. EMBO J. 9: 1355–64PubMedGoogle Scholar
  38. Magasanik B (1989) Regulation of transcription of theglnALG operon ofE. coli by protein phosphorylation. Biochime 71: 1005–1012Google Scholar
  39. Martin DIK & Orkin SH (1990) Transcriptional activation and DNA-binding by the erythroid factor GF-1/NF-E1/Eryfl. Gen. Devel. 4: 1886–1898Google Scholar
  40. Marzluf GA (1981) Regulation of nitrogen metabolisem and gene expression in fungi. Microbiol. Rev. 45: 437–461PubMedGoogle Scholar
  41. Marzluf GA (1993) Regulation of sulfur and nitrogen metabolism in filamentous fungi. Ann. Rev. Microbiol. 47: 31–55Google Scholar
  42. Merika M & Orkin SH (1993). DNA-binding specificity of GATA family transcription factors. Mol. Cell. Biol. 13: 3999–4010PubMedGoogle Scholar
  43. Minehart PL & Magasanik B (1991) Sequence and expression of GLN3, a positive nitrogen regulatory gene ofSaccharomyces cerevisiae encoding a protein with a putative zinc finger DNA-binding domain. Mol. Cell. Biol. 11: 6216–6228PubMedGoogle Scholar
  44. Moll T, Tebb G, Surana U, Robitsch H & Nasmyth K (1991) The Role of Phosphorylation and the CDC28 Protein Kinase in Cell Cycle-Regulated Nuclear Import of theS. cerevisiae Transcription Factor SW15. Cell 66: 743–758PubMedGoogle Scholar
  45. Omichinski JG, Trainor C, Evans T Gronenborn AM, Clore GM & Felsenfeld G (1993a). A small single-‘finger’ peptide from the erythroid transcription factor GATA-1 binds specifically to DNA as a zinc or iron complex. Proc. Natl. Acad. Sci. USA 90: 1676–1680PubMedGoogle Scholar
  46. Omichinski JG, Clore GM, Schaad O, Felsenfeld G, Trainor C, Appella E, Stahl SJ & Gronenborn AM (1993b) NMR Structure of a Specific DNA Complex of Zn-Containing DNA Binding Domain of GATA-1. Science 261: 438–446Google Scholar
  47. Orkin SH (1992) GATA-binding transcription factors in haematopoietic cells. Blood 80: 575–581PubMedGoogle Scholar
  48. Peters B, Merezhinskaya N, Diffley JFX & Noguchi CT (1993) Protein-DNA interactions in the — globin gene silencer. J. Biol. Chem. 268(5): 3430–3437PubMedGoogle Scholar
  49. Rai R, Genbauffe FS, Sumrada RA & Cooper TG (1989) Identification of sequences responsible for transcriptional activation of the allantoate permease gene in Saccharomyces cerevisiae. Mol. Cell Biol. 9: 602–608PubMedGoogle Scholar
  50. Shaffer PM & Arst HN Jr (1984) Regulation of pyrimidine salvage inAspergillus nidulans: A role for the major regulatory geneareA mediating nitrogen metabolite repression. Mol. Gen. Genet. 198: 139–145PubMedGoogle Scholar
  51. Shaffer PM, Arst HN Jr Estberg L, Fernando L, Ly T & Sitter M (1988) An asparaginase ofAspergillus nidulans is subject to oxygen repression in addition to nitrogen metabolite repression. Mol. Gen. Genet. 212: 337–341PubMedGoogle Scholar
  52. Spieth J, Shim YH, Conrad R & Blumenthal T (1991)elt-1, an embryologically expressed Caenorhabditis elegans gene homologous to the GATA transcription factor family. Mol. Cell. Biol. 11(9): 4651–4659PubMedGoogle Scholar
  53. Stankovich M, Platt A, Caddick MX, Langdon T, Shaffer, PM & Arst HN Jr (1993). C-terminal truncation of the transcriptional activator encoded byareA inAspergillus nidulans results in both loss-of-function and gain-of-function phenotypes. Mol. Microbiol. 7: 81–87PubMedGoogle Scholar
  54. Tollervey DW (1981) Aspects of nitrogen metabolic regulation inAspergillus nidulans. Ph.D. Thesis, University of CambridgeGoogle Scholar
  55. Tollervey DW & Arst HN Jr (1981) Mutations to constitutivity and derepression are separate and separable in a regulatory gene ofAspergillus nidulans. Curr. Genet. 4: 63–68Google Scholar
  56. Tollervey DW & Arst HN Jr (1982) Domain-wide locus-specific suppression of nitrogen metabolite represed mutations ofAspergillus nidulans. Curr. Genet. 6: 79–85Google Scholar
  57. Trainor CC, Evans J, Felsenfeld G & Boguski MS (1990). Structure and evolution of a human erythroid transcription factor. Nature (London) 343: 92–96PubMedGoogle Scholar
  58. Tsai SF, Martin DI, Zon LI, DAndrea AD, Wong GG & Orkin SH (1989) Cloning of the cDNA for the major DNA-binding protein of the erythroid lineage through expression in mammalian cells. Nature (London) 339: 446–451PubMedGoogle Scholar
  59. Voisard C, Wang j, McEvoy, Xu P & Leong SA (1993)urbs1 a gene regulating siderophore biosynthesis inUstilago maydis, encodes a protein similar to the erythroid transcription factor GATA-1. Mol. Cell. Biol. 13: 7091–7100PubMedGoogle Scholar
  60. Wiame JM, Grenson M & Arst HN Jr (1985) Nitrogen catabolite repression in yeasts and filamentous fungi. Adv. Microbiol. Physiol. 26: 1–87Google Scholar
  61. Yamamoto M, Ko LJ, Leonard MW, Beug H, Orkin SH & Engel JD (1990) Activity and tissue specific expression of the transcription factor NF-E1 multigene family. Gen. Devel. 4: 1650–1662Google Scholar
  62. Yang H-Y & Evans, T (1992) Distinct roles for the two cGATA-1 finger domains. Mol. Cell. Biol. 12: 4562–4570PubMedGoogle Scholar
  63. Young JL, Jaran G, Fu Y-H & Marzluf GA (1990) Nucleotide sequence and analysis of NMR, a negative-acting regulatory gene in the nitrogen circuit ofNeurospora crassa. Mol. Gen. Genet. 222: 120–128PubMedGoogle Scholar
  64. Young JL & Marzluf GA (1991) Molecular comparison of the negative-acting nitrogen control gene,nmr, inNeurosporacrassa and otherNeurospora and fungal species. Biochem. Genet. 29: 447–459PubMedGoogle Scholar
  65. Zon LI, Tsai S-F, Burgess S, Bolce ME, Harland RM & Orkin SH. (1990) The major human erythroid DNA binding protein (GF-1; NF-E1; Eryf-1): Primary sequence and localization of the gene to the X chromosome. Proc. Natl. Acad. Sci. USA 87: 668–672PubMedGoogle Scholar
  66. Zon LI, Mather C, Burgess S, Bolce ME, Harland RM & Orkin SH (1991) Expression of GATA-binding proteins during embryonic development inXenopus laevis. Proc. Natl. Acad. Sci. USA 88: 10642–10646PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Mark X. Caddick
    • 1
  • David Peters
    • 1
  • Adam Platt
    • 1
  1. 1.Department of Genetics and Microbiology, Donnan LaboratoriesUniversity of LiverpoolLiverpoolUK

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