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Expression of the carG gene, encoding geranylgeranyl pyrophosphate synthase, is up-regulated by blue light in Mucor circinelloides

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Abstract

A new structural gene, carG, involved in the biosynthesis of carotenoids in the fungus Mucor circinelloides was isolated by heterologous hybridisation, using a probe derived from the Gibberella fujikuroi ggs1 gene. Functional analyses in Escherichia coli showed that the encoded protein has geranylgeranyl pyrophosphate (GGPP) synthase activity. A comparison of the deduced protein with other GGPP synthases suggested that the carG gene might have evolved from other larger genes present in some fungi. The analysis of carG mRNA accumulation after blue light irradiation showed that the expression of this gene is up-regulated by blue light, as happens with the other structural genes involved in carotenogenesis in M. circinelloides. Analysis of the promoter region revealed the presence of several APE-like sequences, which participate in the blue-light regulation of the expression of different fungal genes. These sequences are also present in the above-mentioned Mucor genes and strongly support the idea that this gene plays an important role in the regulation of carotenoid synthesis, despite belonging to a more general metabolic pathway.

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References

  • Ballario P, Macino G (1997) White collar proteins: PASsing the light signal in Neurospora crassa. Trends Microbiol 5:458–462

    CAS  PubMed  Google Scholar 

  • Blasco JL, García-Sánchez MA, Ruiz-Herrera J, Eslava AP, Iturriaga EA (2002) A gene coding for ornithine decarboxylase (odcA) is differentially expressed during the Mucor circinelloides yeast-to-hypha transition. Res Microbiol 153:155–164

    Article  CAS  PubMed  Google Scholar 

  • Burke C, Croteau R (2002) Interaction with the small subunit of geranyl diphosphate synthase modifies the chain length specificity of geranylgeranyl diphosphate synthase to produce geranyl diphosphate. J Biol Chem 277:3141–3149

    Article  CAS  PubMed  Google Scholar 

  • Carattoli A, Cogoni C, Morelli G, Macino G (1994) Molecular characterization of upstream regulatory sequences controlling the photoinduced expression of the albino-3 gene of Neurospora crassa. Mol Microbiol 13:787–795

    CAS  PubMed  Google Scholar 

  • Cerdá-Olmedo E, Corrochano LM (1996) Photoregulation of fungal gene expression. In: Jennings RC, Zucchelli G, Ghetti F, Colombetti G (eds) Light as an energy source and information carrier in plant physiology. Plenum Press, New York, pp 285–292

  • Díaz-Mínguez JM, Iturriaga EA, Benito EP, Corrochano LM, Eslava AP (1990) Isolation and molecular analysis of the orotidine-5'-monophosphate decarboxylase gene (pyrG) of Phycomyces blakesleeanus. Mol Gen Genet 224:269–278

    PubMed  Google Scholar 

  • Fraser PD, Ruiz-Hidalgo MJ, López-Matas MA, Álvarez MI, Eslava AP, Bramley PM (1996) Carotenoid biosynthesis in wild-type and mutant strains of Mucor circinelloides. Biochim Biophys Acta 1289:203–208

    Article  CAS  PubMed  Google Scholar 

  • Gelf MH, Scholten JD, Sebolt-Leopold JS (1998) Protein prenylation: from discovery to prospects for cancer treatment. Curr Opin Chem Biol 2:40–48

    Article  PubMed  Google Scholar 

  • Hirooka K, Kato T, Matsu-ura J, Hemmi H, Nishino T (2000) The role of histidine-114 of Sulfolobus acidocaldarius geranylgeranyl diphosphate synthase in chain-length determination. FEBS Lett 481:68–72

    Article  CAS  Google Scholar 

  • Iturriaga EA, Díaz-Mínguez JM, Benito EP, Alvarez MI, Eslava AP (1992) Heterologous transformation of Mucor circinelloides with the Phycomyces blakesleeanus leu1 gene. Curr Genet 21:215–223

    PubMed  Google Scholar 

  • Iturriaga EA, Velayos A, Eslava AP (2000) The structure and function of the genes involved in the biosynthesis of carotenoids in the Mucorales. Biotechnol Bioprocess Eng 5:263–274

    CAS  Google Scholar 

  • Kellogg BA, Poulter CD (1997) Chain elongation in the isoprenoid biosynthetic pathway. Curr Opin Chem Biol 1:570–578

    Article  CAS  Google Scholar 

  • Linden H, Ballario P, Macino G (1997) Blue light regulation in Neurospora crassa. Fungal Genet Biol 22:141–150

    CAS  PubMed  Google Scholar 

  • Lütke-Brinkhaus FL, Rilling HC (1988) Purification of geranylgeranyl diphosphate synthase from Phycomyces blakesleanus. Arch Biochem Biophys 266:607–612

    PubMed  Google Scholar 

  • Mende K, Homann V, Tudzynski B (1997) The geranylgeranyl diphosphate synthase gene of Gibberella fujikuroi: isolation and expression. Mol Gen Genet 255:96–105

    CAS  PubMed  Google Scholar 

  • Misawa N, Nakagawa M, Kobayashi K, Yamano S, Izawa Y, Nakamura K, Harashima K (1990) Elucidation of the Erwinia uredovora carotenoid biosynthetic pathway by functional analysis of gene products expressed in Escherichia coli. J Bacteriol 172:6704–6712

    CAS  PubMed  Google Scholar 

  • Möller EM, Bahnweg G, Sandermann H, Geiger HH (1992) A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies, and infected plant tissues. Nucleic Acids Res 20:6115–6116

    PubMed  Google Scholar 

  • Navarro E, Sandmann G, Torres-Martínez S (1995) Mutants of the carotenoid pathway of Mucor circinelloides. Exp Mycol 19:186–190

    Article  CAS  Google Scholar 

  • Nelson MA, Morelli G, Carattoli A, Romano N, Macino G (1989) Molecular cloning of a Neurospora crassa carotenoid biosynthetic gene (albino-3) regulated by blue light and the products of the white collar genes. Mol Cell Biol 9:1271–1276

    CAS  PubMed  Google Scholar 

  • Ogura K, Koyama T (1998) Enzymatic aspects of isoprenoid chain elongation. Chem Rev 98:1263–1276

    CAS  PubMed  Google Scholar 

  • Ohnuma S, Hirooka K, Tsuruoka N, Yano M, Ohto C, Nakane H, Nishino T (1998) A pathway where polyprenyl diphosphate elongates in prenyltransferase. Insight into a common mechanism of chain length determination of prenyltransferases. J Biol Chem 273:26705–26713

    Article  CAS  Google Scholar 

  • Ruiz-Hidalgo MJ, Benito EP, Sandmann G, Eslava AP (1997) The phytoene dehydrogenase gene of Phycomyces: regulation of its expression by blue light and vitamin A. Mol Gen Genet 253:734–744

    CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.

    Google Scholar 

  • Schmidhauser TJ, Lauter FR, Russo VEA, Yanofsky C (1990) Cloning, sequence and photoregulation of al-1, a carotenoid biosynthetic gene of Neurospora crassa. Mol Cell Biol 10:5064–5070

    CAS  PubMed  Google Scholar 

  • Schmidhauser TJ, Lauter FR, Schumacher M, Zhou WB, Russo VEA, Yanofsky C (1994) Characterization of al-2, the phytoene synthase gene of Neurospora crassa. J Biol Chem 269:12060–12066

    CAS  PubMed  Google Scholar 

  • Tudzynski B, Hölter K (1998) Gibberellin biosynthetic pathway in Gibberella fujikuroi: evidence for a gene cluster. Fungal Genet Biol 25:157–170

    CAS  PubMed  Google Scholar 

  • Unkles SE (1992) Gene organization in industrial filamentous fungi. In: Kinghorn JR, Turner G (eds) Applied molecular genetics of filamentous fungi. Blackie Academic & Professional, Glasgow, pp 28–53

  • Velayos A (2001) Carotenogénesis en Mucor circinelloides. PhD thesis, Universidad de Salamanca, Salamanca

  • Velayos A, López-Matas MA, Ruiz-Hidalgo MJ, Eslava AP (1997) Complementation analysis of carotenogenic mutants of Mucor circinelloides. Fungal Genet Biol 22:19–27

    CAS  PubMed  Google Scholar 

  • Velayos A, Alvarez MI, Eslava, AP, Iturriaga EA (1998) Interallelic complementation at the pyrF locus and the homodimeric nature of orotate phosphoribosyltransferase (OPRTase) in Mucor circinelloides. Mol Gen Genet 260:251–260

    Article  CAS  Google Scholar 

  • Velayos A, Blasco JL, Alvarez MI, Iturriaga EA, Eslava AP (2000a) Blue-light regulation of the phytoene dehydrogenase (carB) gene expression in Mucor circinelloides. Planta 210:938–946

    CAS  PubMed  Google Scholar 

  • Velayos A, Eslava AP, Iturriaga EA (2000b) A bifunctional enzyme with lycopene cyclase and phytoene synthase activities is encoded by the carRP gene of Mucor circinelloides. Eur J Biochem 267:5509–5519

    Article  CAS  PubMed  Google Scholar 

  • Vittorioso P, Carattoli A, Londei P, Macino G (1994) Internal translational initiation in the mRNA from the Neurospora crassa Albino-3 gene. J Biol Chem 269:26650–26654

    CAS  Google Scholar 

  • Wang K, Ohnuma S (1999) Chain-length determination mechanism of isoprenyl diphosphate synthases and implications for molecular evolution. Trends Biochem Sci 24:445–451

    CAS  PubMed  Google Scholar 

  • Young C, McMillan L, Telfer E, Scott B (2001) Molecular cloning and genetic analysis of an indole–diterpene cluster from Penicillium paxilli. Mol Microbiol 39:754–764

    CAS  PubMed  Google Scholar 

  • Zhu XF, Suzuki K, Saito T, Okada K, Tanaka K, Nakagawa T, Matsuda H, Kawamukai M (1997) Geranylgeranyl pyrophosphate synthase encoded by the newly isolated gene GGPP6 from Arabidopsis thaliana is localized in mitochondria. Plant Mol Biol 35:331–341

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank Dr. B. Tudzynski for kindly providing the G. fujikuroi pGGPP plasmid. This work was supported by grants PB97-1307 (Ministerio de Educación y Cultura, Spain), IFD97-1476 (Fondos FEDER, Ministerio de Educación y Cultura, Spain) and SA067/01 (Junta de Castilla y León). A.V. held a graduate fellowship from the Ministerio de Educación y Cultura.

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  1. Antonio Velayos

    Present address: Neurogenetics Group, The Wellcome Trust Centre for Human Genetics, Roosevelt Drive, Oxford, OX3 7BN, UK

Authors and Affiliations

  1. Área de Genética, Departamento de Microbiología y Genética, Universidad de Salamanca, Avenida del Campo Charro s/n, 37007, Salamanca, Spain

    Antonio Velayos, Tamás Papp, Raúl Aguilar-Elena, Mónica Fuentes-Vicente, Enrique A. Iturriaga & María Isabel Álvarez

  2. Centro Hispano-Luso de Investigaciones Agrarias, Universidad de Salamanca, Avenida del Campo Charro s/n, 37007, Salamanca, Spain

    Arturo P. Eslava

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  1. Antonio Velayos
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Correspondence to Enrique A. Iturriaga.

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Communicated by U. Kück

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Velayos, A., Papp, T., Aguilar-Elena, R. et al. Expression of the carG gene, encoding geranylgeranyl pyrophosphate synthase, is up-regulated by blue light in Mucor circinelloides . Curr Genet 43, 112–120 (2003). https://doi.org/10.1007/s00294-003-0376-5

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