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11 Regulation of Fungal Nitrogen Metabolism

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Biochemistry and Molecular Biology

Part of the book series: The Mycota ((MYCOTA,volume III))

Abstract

Genes for nitrogen acquisition and metabolism are highly regulated in filamentous fungi for adaptation to changes in nitrogen nutrient availability. Much of our understanding of the regulatory mechanisms comes from studies in the models Aspergillus nidulans, Neurospora crassa, and Fusarium fujikuroi. The last decade has seen many advances in this field including our understanding of the mechanisms controlling action of the key nitrogen transcription factor AreA, as well as new insights into the roles of other components of the global nitrogen regulatory system. This chapter will review these advances with a focus on the work in A. nidulans.

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References

  • Andrianopoulos A, Hynes MJ (1990) Sequence and functional analysis of the positively acting regulatory gene amdR from Aspergillus nidulans. Mol Cell Biol 10:3194–3203

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Andrianopoulos A, Kourambas S, Sharp JA, Davis MA, Hynes MJ (1998) Characterization of the Aspergillus nidulans nmrA gene involved in nitrogen metabolite repression. J Bacteriol 180:1973–1977

    PubMed Central  PubMed  CAS  Google Scholar 

  • Arst HN Jr, Bailey CR (1980) Genetic evidence for a second asparaginase in Aspergillus nidulans. J Gen Microbiol 121:243–247

    PubMed  CAS  Google Scholar 

  • Arst HN Jr, Cove DJ (1973) Nitrogen metabolite repression in Aspergillus nidulans. Mol Gen Genet 126:111–141

    Article  PubMed  CAS  Google Scholar 

  • Arst HN, Brownlee AG, Cousen SA (1982) Nitrogen metabolite repression in Aspergillus nidulans – a farewell to tamA? Curr Genet 6:245–257

    Article  PubMed  CAS  Google Scholar 

  • Beck T, Hall MN (1999) The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402:689–692

    Article  PubMed  CAS  Google Scholar 

  • Berger H, Pachlinger R, Morozov I, Goller S, Narendja F, Caddick M, Strauss J (2006) The GATA factor AreA regulates localization and in vivo binding site occupancy of the nitrate activator NirA. Mol Microbiol 59:433–446

    Article  PubMed  CAS  Google Scholar 

  • Berger H, Basheer A, Bock S, Reyes-Dominguez Y, Dalik T, Altmann F, Strauss J (2008) Dissecting individual steps of nitrogen transcription factor cooperation in the Aspergillus nidulans nitrate cluster. Mol Microbiol 69:1385–1398

    Article  PubMed  CAS  Google Scholar 

  • Bernreiter A, Ramon A, Fernandez-Martinez J, Berger H, Araujo-Bazan L, Espeso EA, Pachlinger R, Gallmetzer A, Anderl I, Scazzocchio C, Strauss J (2007) Nuclear export of the transcription factor NirA is a regulatory checkpoint for nitrate induction in Aspergillus nidulans. Mol Cell Biol 27:791–802

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bertram PG, Choi JH, Carvalho J, Ai W, Zeng C, Chan TF, Zheng XF (2000) Tripartite regulation of Gln3p by TOR, Ure2p, and phosphatases. J Biol Chem 275:35727–35733

    Article  PubMed  CAS  Google Scholar 

  • Bricmont PA, Daugherty JR, Cooper TG (1991) The DAL81 gene product is required for induced expression of two differently regulated nitrogen catabolic genes in Saccharomyces cerevisiae. Mol Cell Biol 11:1161–1166

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bugeja HE, Hynes MJ, Andrianopoulos A (2012) AreA controls nitrogen source utilisation during both growth programs of the dimorphic fungus Penicillium marneffei. Fungal Biol 116:145–154

    Article  PubMed  CAS  Google Scholar 

  • Burger G, Strauss J, Scazzocchio C, Lang BF (1991) nirA, the pathway-specific regulatory gene of nitrate assimilation in Aspergillus nidulans, encodes a putative GAL4-type zinc finger protein and contains four introns in highly conserved regions. Mol Cell Biol 11:5746–5755

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Caddick MX (2004) Nitrogen regulation in mycelial fungi. In: Brambl R, Marzluf GA (eds) The Mycota: biochemistry and molecular biology, vol III, 2nd edn, The Mycota. Springer, Berlin, pp 349–368

    Chapter  Google Scholar 

  • Caddick MX, Jones MG, van Tonder JM, Le Cordier H, Narendja F, Strauss J, Morozov IY (2006) Opposing signals differentially regulate transcript stability in Aspergillus nidulans. Mol Microbiol 62:509–519

    Article  PubMed  CAS  Google Scholar 

  • Cardillo SB, Levi CE, Bermudez Moretti M, Correa Garcia S (2012) Interplay between the transcription factors acting on the GATA- and GABA-responsive elements of Saccharomyces cerevisiae UGA promoters. Microbiology 158:925–935

    Article  PubMed  CAS  Google Scholar 

  • Chang PK, Todd RB (2004) Metabolic pathway regulation. In: Arora DK (ed) Handbook of fungal biotechnology, vol 20, 2nd edn, Mycology series. Marcel Dekker, New York, pp 25–37

    Google Scholar 

  • Chang PK, Yu J, Bhatnagar D, Cleveland TE (2000) Characterization of the Aspergillus parasiticus major nitrogen regulatory gene, areA. Biochim Biophys Acta 1491:263–266

    Article  PubMed  CAS  Google Scholar 

  • Chiang TY, Marzluf GA (1994) DNA recognition by the NIT2 nitrogen regulatory protein: importance of the number, spacing, and orientation of GATA core elements and their flanking sequences upon NIT2 binding. Biochemistry 33:576–582

    Article  PubMed  CAS  Google Scholar 

  • Christensen T, Hynes MJ, Davis MA (1998) Role of the regulatory gene areA of Aspergillus oryzae in nitrogen metabolism. Appl Environ Microbiol 64:3232–3237

    PubMed Central  PubMed  CAS  Google Scholar 

  • Coleman M, Henricot B, Arnau J, Oliver RP (1997) Starvation-induced genes of the tomato pathogen Cladosporium fulvum are also induced during growth in planta. Mol Plant Microbe Interact 10:1106–1109

    Article  PubMed  CAS  Google Scholar 

  • Conlon H, Zadra I, Haas H, Arst HN Jr, Jones MG, Caddick MX (2001) The Aspergillus nidulans GATA transcription factor gene areB encodes at least three proteins and features three classes of mutation. Mol Microbiol 40:361–375

    Article  PubMed  CAS  Google Scholar 

  • Cooper TG (2002) Transmitting the signal of excess nitrogen in Saccharomyces cerevisiae from the Tor proteins to the GATA factors: connecting the dots. FEMS Microbiol Rev 26:223–238

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Davis MA, Hynes MJ (2004) Regulation of the amdS gene in Aspergillus nidulans. In: Brambl R, Marzluf GA (eds) The Mycota III. Biochemistry and molecular biology (2nd edn). Springer, Berlin

    Google Scholar 

  • Davis MA, Small AJ, Kourambas S, Hynes MJ (1996) The tamA gene of Aspergillus nidulans contains a putative zinc cluster motif which is not required for gene function. J Bacteriol 178:3406–3409

    PubMed Central  PubMed  CAS  Google Scholar 

  • Denu JM (2003) Linking chromatin function with metabolic networks: Sir2 family of NAD(+)-dependent deacetylases. Trends Biochem Sci 28:41–48

    Article  PubMed  CAS  Google Scholar 

  • Divon HH, Rothan-Denoyes B, Davydov O, Dip A, Fluhr R (2005) Nitrogen-responsive genes are differentially regulated in planta during Fusarium oxyspsorum f. sp. lycopersici infection. Mol Plant Pathol 6:459–470

    Article  PubMed  CAS  Google Scholar 

  • Donofrio NM, Oh Y, Lundy R, Pan H, Brown DE, Jeong JS, Coughlan S, Mitchell TK, Dean RA (2006) Global gene expression during nitrogen starvation in the rice blast fungus, Magnaporthe grisea. Fungal Genet Biol 43:605–617

    Article  PubMed  CAS  Google Scholar 

  • Downes DJ, Davis MA, Kreutzberger SD, Taig BL, Todd RB (2013) Regulation of the NADP-glutamate dehydrogenase gene gdhA in Aspergillus nidulans by the Zn(II)2Cys6 transcription factor LeuB. Microbiology 159:2467–2480

    Article  PubMed  CAS  Google Scholar 

  • Downes DJ, Chonofsky M, Tan K, Pfannenstiel BT, Reck-Peterson SL, Todd RB (2014a) Characterization of the mutagenic spectrum of 4-nitroquinoline 1-oxide (4-NQO) in Aspergillus nidulans by whole genome sequencing. G3 Bethesda 4:2483–2492

    Article  PubMed Central  PubMed  Google Scholar 

  • Downes DJ, Davis MA, Wong KH, Kreutzberger SD, Hynes MJ, Todd RB (2014b) Dual DNA binding and coactivator functions of Aspergillus nidulans TamA, a Zn(II)2Cys6 transcription factor. Mol Microbiol 92(6):1198–211

    Article  PubMed  CAS  Google Scholar 

  • Dzikowska A, Kacprzak M, Tomecki R, Koper M, Scazzocchio C, Weglenski P (2003) Specific induction and carbon/nitrogen repression of arginine catabolism gene of Aspergillus nidulans--functional in vivo analysis of the otaA promoter. Fungal Genet Biol 38:175–186

    Article  PubMed  CAS  Google Scholar 

  • Empel J, Sitkiewicz I, Andrukiewicz A, Lasocki K, Borsuk P, Weglenski P (2001) arcA, the regulatory gene for the arginine catabolic pathway in Aspergillus nidulans. Mol Genet Genomics 266:591–597

    Article  PubMed  CAS  Google Scholar 

  • Feng B, Marzluf GA (1998) Interaction between major nitrogen regulatory protein NIT2 and pathway-specific regulatory factor NIT4 is required for their synergistic activation of gene expression in Neurospora crassa. Mol Cell Biol 18:3983–3990

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Feng B, Haas H, Marzluf GA (2000) ASD4, a new GATA factor of Neurospora crassa, displays sequence-specific DNA binding and functions in ascus and ascospore development. Biochemistry 39:11065–11073

    Article  PubMed  CAS  Google Scholar 

  • Fernandes L, Rodrigues-Pousada C, Struhl K (1997) Yap, a novel family of eight bZIP proteins in Saccharomyces cerevisiae with distinct biological functions. Mol Cell Biol 17:6982–6993

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fernandez J, Wright JD, Hartline D, Quispe CF, Madayiputhiya N, Wilson RA (2012) Principles of carbon catabolite repression in the rice blast fungus: Tps1, Nmr1-3, and a MATE-family pump regulate glucose metabolism during infection. PLoS Genet 8:e1002673

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fitzgibbon GJ, Morozov IY, Jones MG, Caddick MX (2005) Genetic analysis of the TOR pathway in Aspergillus nidulans. Eukaryot Cell 4:1595–1598

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fraser JA, Davis MA, Hynes MJ (2001) The formamidase gene of Aspergillus nidulans: regulation by nitrogen metabolite repression and transcriptional interference by an overlapping upstream gene. Genetics 157:119–131

    PubMed Central  PubMed  CAS  Google Scholar 

  • Fraser JA, Davis MA, Hynes MJ (2002) A gene from Aspergillus nidulans with similarity to URE2 of Saccharomyces cerevisiae encodes a glutathione S-transferase which contributes to heavy metal and xenobiotic resistance. Appl Environ Microbiol 68:2802–2808

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Froeliger EH, Carpenter BE (1996) NUT1, a major nitrogen regulatory gene in Magnaporthe grisea, is dispensable for pathogenicity. Mol Gen Genet 251:647–656

    PubMed  CAS  Google Scholar 

  • Fu YH, Marzluf GA (1990) nit-2, the major nitrogen regulatory gene of Neurospora crassa, encodes a protein with a putative zinc finger DNA-binding domain. Mol Cell Biol 10:1056–1065

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fu YH, Young JL, Marzluf GA (1988) Molecular cloning and characterization of a negative-acting nitrogen regulatory gene of Neurospora crassa. Mol Gen Genet 214:74–79

    Article  PubMed  CAS  Google Scholar 

  • Gacek A, Strauss J (2012) The chromatin code of fungal secondary metabolite gene clusters. Appl Microbiol Biotechnol 95:1389–1404

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Garcia I, Gonzalez R, Gomez D, Scazzocchio C (2004) Chromatin rearrangements in the prnD-prnB bidirectional promoter: dependence on transcription factors. Eukaryot Cell 3:144–156

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gomez D, Garcia I, Scazzocchio C, Cubero B (2003) Multiple GATA sites: protein binding and physiological relevance for the regulation of the proline transporter gene of Aspergillus nidulans. Mol Microbiol 50:277–289

    Article  PubMed  CAS  Google Scholar 

  • Haas H, Bauer B, Redl B, Stoffler G, Marzluf GA (1995) Molecular cloning and analysis of nre, the major nitrogen regulatory gene of Penicillium chrysogenum. Curr Genet 27:150–158

    Article  PubMed  CAS  Google Scholar 

  • Haas H, Angermayr K, Zadra I, Stoffler G (1997) Overexpression of nreB, a new GATA factor-encoding gene of Penicillium chrysogenum, leads to repression of the nitrate assimilatory gene cluster. J Biol Chem 272:22576–22582

    Article  PubMed  CAS  Google Scholar 

  • Horst RJ, Zeh C, Saur A, Sonnewald S, Sonnewald U, Voll LM (2012) The Ustilago maydis Nit2 homolog regulates nitrogen utilization and is required for efficient induction of filamentous growth. Eukaryot Cell 11:368–380

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hunter CC, Siebert KS, Downes DJ, Wong KH, Kreutzberger SD, Fraser JA, Clarke DF, Hynes MJ, Davis MA, Todd RB (2014) Multiple nuclear localization signals mediate nuclear localization of the GATA transcription factor AreA. Eukaryot Cell 13:527–538

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kim H, Woloshuk CP (2008) Role of AREA, a regulator of nitrogen metabolism, during colonization of maize kernels and fumonisin biosynthesis in Fusarium verticillioides. Fungal Genet Biol 45:947–953

    Article  PubMed  CAS  Google Scholar 

  • Kim Y, Islam N, Moss BJ, Nandakumar MP, Marten MR (2011) Autophagy induced by rapamycin and carbon-starvation have distinct proteome profiles in Aspergillus nidulans. Biotechnol Bioeng 108:2705–2715

    Article  PubMed  CAS  Google Scholar 

  • Kinghorn JR, Pateman JA (1975) Studies of partially repressed mutants at the tamA and areA loci in Aspergillus nidulans. Mol Gen Genet 140:137–147

    Article  PubMed  CAS  Google Scholar 

  • Kmetzsch L, Staats CC, Simon E, Fonseca FL, Oliveira DL, Joffe LS, Rodrigues J, Lourenco RF, Gomes SL, Nimrichter L, Rodrigues ML, Schrank A, Vainstein MH (2011) The GATA-type transcriptional activator Gat1 regulates nitrogen uptake and metabolism in the human pathogen Cryptococcus neoformans. Fungal Genet Biol 48:192–199

    Article  PubMed  CAS  Google Scholar 

  • Kotaka M, Johnson C, Lamb HK, Hawkins AR, Ren J, Stammers DK (2008) Structural analysis of the recognition of the negative regulator NmrA and DNA by the zinc finger from the GATA-type transcription factor AreA. J Mol Biol 381:373–382

    Article  PubMed  CAS  Google Scholar 

  • Krol K, Morozov IY, Jones MG, Wyszomirski T, Weglenski P, Dzikowska A, Caddick MX (2013) RrmA regulates the stability of specific transcripts in response to both nitrogen source and oxidative stress. Mol Microbiol 89:975–988

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kudla B, Caddick MX, Langdon T, Martinez-Rossi NM, Bennett CF, Sibley S, Davies RW, Arst HN Jr (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

    PubMed Central  PubMed  CAS  Google Scholar 

  • Kudo N, Matsumori N, Taoka H, Fujiwara D, Schreiner EP, Wolff B, Yoshida M, Horinouchi S (1999) Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc Natl Acad Sci USA 96:9112–9117

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kuge S, Jones N (1994) YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides. EMBO J 13:655–664

    PubMed Central  PubMed  CAS  Google Scholar 

  • Lamb HK, Leslie K, Dodds AL, Nutley M, Cooper A, Johnson C, Thompson P, Stammers DK, Hawkins AR (2003) The negative transcriptional regulator NmrA discriminates between oxidized and reduced dinucleotides. J Biol Chem 278:32107–32114

    Article  PubMed  CAS  Google Scholar 

  • Lamb HK, Ren J, Park A, Johnson C, Leslie K, Cocklin S, Thompson P, Mee C, Cooper A, Stammers DK, Hawkins AR (2004) Modulation of the ligand binding properties of the transcription repressor NmrA by GATA-containing DNA and site-directed mutagenesis. Protein Sci 13:3127–3138

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Langdon T, Sheerins A, Ravagnani A, Gielkens M, Caddick MX, Arst HN Jr (1995) Mutational analysis reveals dispensability of the N-terminal region of the Aspergillus transcription factor mediating nitrogen metabolite repression. Mol Microbiol 17:877–888

    Article  PubMed  CAS  Google Scholar 

  • Lee IR, Chow EW, Morrow CA, Djordjevic JT, Fraser JA (2011) Nitrogen metabolite repression of metabolism and virulence in the human fungal pathogen Cryptococcus neoformans. Genetics 188:309–323

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lee IR, Lim JW, Ormerod KL, Morrow CA, Fraser JA (2012) Characterization of an Nmr homolog that modulates GATA factor-mediated nitrogen metabolite repression in Cryptococcus neoformans. PLoS One 7, e32585

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lopez-Berges MS, Rispail N, Prados-Rosales RC, Di Pietro A (2010a) A nitrogen response pathway regulates virulence functions in Fusarium oxysporum via the protein kinase TOR and the bZIP protein MeaB. Plant Cell 22:2459–2475

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lopez-Berges MS, Rispail N, Prados-Rosales RC, Di Pietro A (2010b) A nitrogen response pathway regulates virulence in plant pathogenic fungi: role of TOR and the bZIP protein MeaB. Plant Signal Behav 5:1623–1625

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • MacCabe AP, Vanhanen S, Sollewign Gelpke MD, van de Vondervoort PJ, Arst HN Jr, Visser J (1998) Identification, cloning and sequence of the Aspergillus niger areA wide domain regulatory gene controlling nitrogen utilisation. Biochim Biophys Acta 1396:163–168

    Article  PubMed  CAS  Google Scholar 

  • Macios M, Caddick MX, Weglenski P, Scazzocchio C, Dzikowska A (2012) The GATA factors AREA and AREB together with the co-repressor NMRA, negatively regulate arginine catabolism in Aspergillus nidulans in response to nitrogen and carbon source. Fungal Genet Biol 49:189–198

    Article  PubMed  CAS  Google Scholar 

  • MacPherson S, Larochelle M, Turcotte B (2006) A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol Mol Biol Rev 70:583–604

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Margelis S, D'Souza C, Small AJ, Hynes MJ, Adams TH, Davis MA (2001) Role of glutamine synthetase in nitrogen metabolite repression in Aspergillus nidulans. J Bacteriol 183:5826–5833

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Marzluf GA (1997) Genetic regulation of nitrogen metabolism in the fungi. Microbiol Mol Biol Rev 61:17–32

    PubMed Central  PubMed  CAS  Google Scholar 

  • Michielse CB, Pfannmuller A, Macios M, Rengers P, Dzikowska A, Tudzynski B (2014) The interplay between the GATA transcription factors AreA, the global nitrogen regulator and AreB in Fusarium fujikuroi. Mol Microbiol 91:472–493

    Article  PubMed  CAS  Google Scholar 

  • Mihlan M, Homann V, Liu TW, Tudzynski B (2003) AREA directly mediates nitrogen regulation of gibberellin biosynthesis in Gibberella fujikuroi, but its activity is not affected by NMR. Mol Microbiol 47:975–991

    Article  PubMed  CAS  Google Scholar 

  • Min K, Shin Y, Son H, Lee J, Kim JC, Choi GJ, Lee YW (2012) Functional analyses of the nitrogen regulatory gene areA in Gibberella zeae. FEMS Microbiol Lett 334:66–73

    Article  PubMed  CAS  Google Scholar 

  • Monahan BJ, Fraser JA, Hynes MJ, Davis MA (2002) Isolation and characterization of two ammonium permease genes, meaA and mepA, from Aspergillus nidulans. Eukaryot Cell 1:85–94

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Monahan BJ, Askin MC, Hynes MJ, Davis MA (2006) Differential expression of Aspergillus nidulans ammonium permease genes is regulated by GATA transcription factor AreA. Eukaryot Cell 5:226–237

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Morozov IY, Martinez MG, Jones MG, Caddick MX (2000) A defined sequence within the 3' UTR of the areA transcript is sufficient to mediate nitrogen metabolite signalling via accelerated deadenylation. Mol Microbiol 37:1248–1257

    Article  PubMed  CAS  Google Scholar 

  • Morozov IY, Galbis-Martinez M, Jones MG, Caddick MX (2001) Characterization of nitrogen metabolite signalling in Aspergillus via the regulated degradation of areA mRNA. Mol Microbiol 42:269–277

    Article  PubMed  CAS  Google Scholar 

  • Morozov IY, Jones MG, Razak AA, Rigden DJ, Caddick MX (2010a) CUCU modification of mRNA promotes decapping and transcript degradation in Aspergillus nidulans. Mol Cell Biol 30:460–469

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Morozov IY, Jones MG, Spiller DG, Rigden DJ, Dattenbock C, Novotny R, Strauss J, Caddick MX (2010b) Distinct roles for Caf1, Ccr4, Edc3 and CutA in the co-ordination of transcript deadenylation, decapping and P-body formation in Aspergillus nidulans. Mol Microbiol 76:503–516

    Article  PubMed  CAS  Google Scholar 

  • Muro-Pastor MI, Gonzalez R, Strauss J, Narendja F, Scazzocchio C (1999) The GATA factor AreA is essential for chromatin remodelling in a eukaryotic bidirectional promoter. EMBO J 18:1584–1597

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Muro-Pastor MI, Strauss J, Ramon A, Scazzocchio C (2004) A paradoxical mutant GATA factor. Eukaryot Cell 3:393–405

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Narendja F, Goller SP, Wolschek M, Strauss J (2002) Nitrate and the GATA factor AreA are necessary for in vivo binding of NirA, the pathway-specific transcriptional activator of Aspergillus nidulans. Mol Microbiol 44:573–583

    Article  PubMed  CAS  Google Scholar 

  • Neville M, Rosbash M (1999) The NES-Crm1p export pathway is not a major mRNA export route in Saccharomyces cerevisiae. EMBO J 18:3746–3756

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Niehaus EM, von Bargen KW, Espino JJ, Pfannmuller A, Humpf HU, Tudzynski B (2014) Characterization of the fusaric acid gene cluster in Fusarium fujikuroi. Appl Microbiol Biotechnol 98:1749–1762

    Article  PubMed  CAS  Google Scholar 

  • Oestreicher N, Ribard C, Scazzocchio C (2008) The nadA gene of Aspergillus nidulans, encoding adenine deaminase, is subject to a unique regulatory pattern. Fungal Genet Biol 45:760–775

    Article  PubMed  CAS  Google Scholar 

  • Olszewska A, Krol K, Weglenski P, Dzikowska A (2007) Arginine catabolism in Aspergillus nidulans is regulated by the rrmA gene coding for the RNA-binding protein. Fungal Genet Biol 44:1285–1297

    Article  PubMed  CAS  Google Scholar 

  • Pan H, Feng B, Marzluf GA (1997) Two distinct protein-protein interactions between the NIT2 and NMR regulatory proteins are required to establish nitrogen metabolite repression in Neurospora crassa. Mol Microbiol 26:721–729

    Article  PubMed  CAS  Google Scholar 

  • Pellier AL, Lauge R, Veneault-Fourrey C, Langin T (2003) CLNR1, the AREA/NIT2-like global nitrogen regulator of the plant fungal pathogen Colletotrichum lindemuthianum is required for the infection cycle. Mol Microbiol 48:639–655

    Article  PubMed  CAS  Google Scholar 

  • Perez-Garcia A, Snoeijers SS, Joosten MH, Goosen T, De Wit PJ (2001) Expression of the Avirulence gene Avr9 of the fungal tomato pathogen Cladosporium fulvum is regulated by the global nitrogen response factor NRF1. Mol Plant Microbe Interact 14:316–325

    Article  PubMed  CAS  Google Scholar 

  • Peters DG, Caddick MX (1994) Direct analysis of native and chimeric GATA specific DNA binding proteins from Aspergillus nidulans. Nucleic Acids Res 22:5164–5172

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Philips AS, Kwok JC, Chong BH (2007) Analysis of the signals and mechanisms mediating nuclear trafficking of GATA-4. Loss of DNA binding is associated with localization in intranuclear speckles. J Biol Chem 282:24915–24927

    Article  PubMed  CAS  Google Scholar 

  • Platt A, Langdon T, Arst HN Jr, Kirk D, Tollervey D, Sanchez JM, Caddick MX (1996a) Nitrogen metabolite signalling involves the C-terminus and the GATA domain of the Aspergillus transcription factor AREA and the 3' untranslated region of its mRNA. EMBO J 15:2791–2801

    PubMed Central  PubMed  CAS  Google Scholar 

  • Platt A, Ravagnani A, Arst H Jr, Kirk D, Langdon T, Caddick MX (1996b) Mutational analysis of the C-terminal region of AREA, the transcription factor mediating nitrogen metabolite repression in Aspergillus nidulans. Mol Gen Genet 250:106–114

    PubMed  CAS  Google Scholar 

  • Pokorska A, Drevet C, Scazzocchio C (2000) The analysis of the transcriptional activator PrnA reveals a tripartite nuclear localisation sequence. J Mol Biol 298:585–596

    Article  PubMed  CAS  Google Scholar 

  • Polley SD, Caddick MX (1996) Molecular characterisation of meaB, a novel gene affecting nitrogen metabolite repression in Aspergillus nidulans. FEBS Lett 388:200–205

    Article  PubMed  CAS  Google Scholar 

  • Polotnianka R, Monahan BJ, Hynes MJ, Davis MA (2004) TamA interacts with LeuB, the homologue of Saccharomyces cerevisiae Leu3p, to regulate gdhA expression in Aspergillus nidulans. Mol Genet Genomics 272:452–459

    Article  PubMed  CAS  Google Scholar 

  • Ravagnani A, Gorfinkiel L, Langdon T, Diallinas G, Adjadj E, Demais S, Gorton D, Arst HN Jr, Scazzocchio C (1997) Subtle hydrophobic interactions between the seventh residue of the zinc finger loop and the first base of an HGATAR sequence determine promoter- specific recognition by the Aspergillus nidulans GATA factor AreA. EMBO J 16:3974–3986

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Reyes-Dominguez Y, Narendja F, Berger H, Gallmetzer A, Fernandez-Martin R, Garcia I, Scazzocchio C, Strauss J (2008) Nucleosome positioning and histone H3 acetylation are independent processes in the Aspergillus nidulans prnD-prnB bidirectional promoter. Eukaryot Cell 7:656–663

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ribard C, Scazzocchio C, Oestreicher N (2001) The oxpA5 mutation of Aspergillus nidulans is an allele of adB, the gene encoding adenylosuccinate synthetase. Mol Genet Genomics 266:701–710

    Article  PubMed  CAS  Google Scholar 

  • Schinko T, Berger H, Lee W, Gallmetzer A, Pirker K, Pachlinger R, Buchner I, Reichenauer T, Guldener U, Strauss J (2010) Transcriptome analysis of nitrate assimilation in Aspergillus nidulans reveals connections to nitric oxide metabolism. Mol Microbiol 78:720–738

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Schönig B, Brown DW, Oeser B, Tudzynski B (2008) Cross-species hybridization with Fusarium verticillioides microarrays reveals new insights into Fusarium fujikuroi nitrogen regulation and the role of AreA and NMR. Eukaryot Cell 7:1831–1846

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sibthorp C, Wu H, Cowley G, Wong PW, Palaima P, Morozov IY, Weedall GD, Caddick MX (2013) Transcriptome analysis of the filamentous fungus Aspergillus nidulans directed to the global identification of promoters. BMC Genomics 14:847

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Small AJ, Hynes MJ, Davis MA (1999) The TamA protein fused to a DNA-binding domain can recruit AreA, the major nitrogen regulatory protein, to activate gene expression in Aspergillus nidulans. Genetics 153:95–105

    PubMed Central  PubMed  CAS  Google Scholar 

  • Small AJ, Todd RB, Zanker MC, Delimitrou S, Hynes MJ, Davis MA (2001) Functional analysis of TamA, a coactivator of nitrogen-regulated gene expression in Aspergillus nidulans. Mol Genet Genomics 265:636–646

    Article  PubMed  CAS  Google Scholar 

  • Snoeijers SS, Vossen P, Goosen T, Van den Broek HW, De Wit PJ (1999) Transcription of the avirulence gene Avr9 of the fungal tomato pathogen Cladosporium fulvum is regulated by a GATA-type transcription factor in Aspergillus nidulans. Mol Gen Genet 261:653–659

    Article  PubMed  CAS  Google Scholar 

  • Stammers DK, Ren J, Leslie K, Nichols CE, Lamb HK, Cocklin S, Dodds A, Hawkins AR (2001) The structure of the negative transcriptional regulator NmrA reveals a structural superfamily which includes the short-chain dehydrogenase/reductases. EMBO J 20:6619–6626

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Starich MR, Wikstrom M, Arst HN Jr, Clore GM, Gronenborn AM (1998a) The solution structure of a fungal AREA protein-DNA complex: an alternative binding mode for the basic carboxyl tail of GATA factors. J Mol Biol 277:605–620

    Google Scholar 

  • Starich MR, Wikstrom M, Schumacher S, Arst HN Jr, Gronenborn AM, Clore GM (1998b) The solution structure of the Leu22-->Val mutant AREA DNA binding domain complexed with a TGATAG core element defines a role for hydrophobic packing in the determination of specificity. J Mol Biol 277:621–634

    Google Scholar 

  • Suarez T, de Queiroz MV, Oestreicher N, Scazzocchio C (1995) The sequence and binding specificity of UaY, the specific regulator of the purine utilization pathway in Aspergillus nidulans, suggest an evolutionary relationship with the PPR1 protein of Saccharomyces cerevisiae. EMBO J 14:1453–1467

    PubMed Central  PubMed  CAS  Google Scholar 

  • Tanzer MM, Arst HN, Skalchunes AR, Coffin M, Darveaux BA, Heiniger RW, Shuster JR (2003) Global nutritional profiling for mutant and chemical mode-of-action analysis in filamentous fungi. Funct Integr Genomics 3:160–170

    Article  PubMed  CAS  Google Scholar 

  • Teichert S, Wottawa M, Schonig B, Tudzynski B (2006) Role of the Fusarium fujikuroi TOR kinase in nitrogen regulation and secondary metabolism. Eukaryot Cell 5:1807–1819

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Teichert S, Rutherford JC, Wottawa M, Heitman J, Tudzynski B (2008) Impact of ammonium permeases mepA, mepB, and mepC on nitrogen-regulated secondary metabolism in Fusarium fujikuroi. Eukaryot Cell 7:187–201

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tessarz P, Kouzarides T (2014) Histone core modifications regulating nucleosome structure and dynamics. Nat Rev Mol Cell Biol 15:703–708

    Article  PubMed  CAS  Google Scholar 

  • Todd RB, Andrianopoulos A (1997) Evolution of a fungal regulatory gene family: the Zn(II)2Cys6 binuclear cluster DNA binding motif. Fungal Genet Biol 21:388–405

    Article  PubMed  CAS  Google Scholar 

  • Todd RB, Greenhalgh JR, Hynes MJ, Andrianopoulos A (2003) TupA, the Penicillium marneffei Tup1p homologue, represses both yeast and spore development. Mol Microbiol 48:85–94

    Article  PubMed  CAS  Google Scholar 

  • Todd RB, Fraser JA, Wong KH, Davis MA, Hynes MJ (2005) Nuclear accumulation of the GATA factor AreA in response to complete nitrogen starvation by regulation of nuclear export. Eukaryot Cell 4:1646–1653

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Todd RB, Zhou M, Ohm RA, Leeggangers HA, Visser L, de Vries RP (2014) Prevalence of transcription factors in ascomycete and basidiomycete fungi. BMC Genomics 15:214

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tollervey DW, Arst HN Jr (1982) Domain-wide, locus-specific suppression of nitrogen metabolite repressed mutations in Aspergillus nidulans. Curr Genet 6:79–85

    Article  PubMed  CAS  Google Scholar 

  • Tudzynski B (2014) Nitrogen regulation of fungal secondary metabolism in fungi. Front Microbiol 5:656

    Article  PubMed Central  PubMed  Google Scholar 

  • Tudzynski B, Homann V, Feng B, Marzluf GA (1999) Isolation, characterization and disruption of the areA nitrogen regulatory gene of Gibberella fujikuroi. Mol Gen Genet 261:106–114

    Article  PubMed  CAS  Google Scholar 

  • Wagner D, Schmeinck A, Mos M, Morozov IY, Caddick MX, Tudzynski B (2010) The bZIP transcription factor MeaB mediates nitrogen metabolite repression at specific loci. Eukaryot Cell 9:1588–1601

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wilson RA, Arst HN Jr (1998) Mutational analysis of AREA, a transcriptional activator mediating nitrogen metabolite repression in Aspergillus nidulans and a member of the “streetwise” GATA family of transcription factors. Microbiol Mol Biol Rev 62:586–596

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wilson RA, Jenkinson JM, Gibson RP, Littlechild JA, Wang ZY, Talbot NJ (2007) Tps1 regulates the pentose phosphate pathway, nitrogen metabolism and fungal virulence. EMBO J 26:3673–3685

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wilson RA, Gibson RP, Quispe CF, Littlechild JA, Talbot NJ (2010) An NADPH-dependent genetic switch regulates plant infection by the rice blast fungus. Proc Natl Acad Sci USA 107:21902–21907

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wong KH, Hynes MJ, Todd RB, Davis MA (2007) Transcriptional control of nmrA by the bZIP transcription factor MeaB reveals a new level of nitrogen regulation in Aspergillus nidulans. Mol Microbiol 66:534–551

    Article  PubMed  CAS  Google Scholar 

  • Wong KH, Hynes MJ, Davis MA (2008) Recent advances in nitrogen regulation: a comparison between Saccharomyces cerevisiae and filamentous fungi. Eukaryot Cell 7:917–925

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wong KH, Hynes MJ, Todd RB, Davis MA (2009) Deletion and overexpression of the Aspergillus nidulans GATA factor AreB reveals unexpected pleiotropy. Microbiology 155:3868–3880

    Article  PubMed  CAS  Google Scholar 

  • Xiao X, Fu YH, Marzluf GA (1995) The negative-acting NMR regulatory protein of Neurospora crassa binds to and inhibits the DNA-binding activity of the positive-acting nitrogen regulatory protein NIT2. Biochemistry 34:8861–8868

    Article  PubMed  CAS  Google Scholar 

  • Zadra I, Abt B, Parson W, Haas H (2000) xylP promoter-based expression system and its use for antisense downregulation of the Penicillium chrysogenum nitrogen regulator NRE. Appl Environ Microbiol 66:4810–4816

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhao X, Hume SL, Johnson C, Thompson P, Huang J, Gray J, Lamb HK, Hawkins AR (2010) The transcription repressor NmrA is subject to proteolysis by three Aspergillus nidulans proteases. Protein Sci 19:1405–1419

    Article  PubMed Central  PubMed  CAS  Google Scholar 

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Acknowledgments

Research in the author’s laboratory has been supported by K-INBRE P20GM103416, Kansas NSF EPSCoR EPS-0903806, Kansas State University Johnson Center for Basic Cancer Research, Kansas State University Plant Biotechnology Center, Australian Research Council grant DP0558002, and the University of Melbourne. Thanks are due to Cameron Hunter and Damien Downes for comments on the manuscript and their contributions to the work. Collaborations with Meryl Davis, Koon Ho Wong, and Michael Hynes are gratefully acknowledged. This is contribution number 15-089-B from the Kansas Agricultural Experiment Station.

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  1. Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA

    Richard B. Todd

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  1. Pharmazeutische Mikrobiologie, Friedrich-Schiller-Universität, Jena, Germany

    Dirk Hoffmeister

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Todd, R.B. (2016). 11 Regulation of Fungal Nitrogen Metabolism. In: Hoffmeister, D. (eds) Biochemistry and Molecular Biology. The Mycota, vol III. Springer, Cham. https://doi.org/10.1007/978-3-319-27790-5_11

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