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Molecular and General Genetics MGG

, Volume 252, Issue 3, pp 223–229 | Cite as

bli-4, a gene that is rapidly induced by blue light, encodes a novel mitochondrial, short-chain alcohol dehydrogenase-like protein inNeurospora crassa

  • J. J. P. Bruchez
  • J. Eberle
  • W. Kohler
  • V. Kruft
  • A. Radford
  • V. E. A. Russo
Original Paper

Abstract

Blue light plays an important role in developmental control throughout nature. Thebli-4 gene ofNeurospora crassa, together withbli-3, al-1 andal-2, is rapidly inducible by blue light. Induction leads to a ninety-fold increase in transcription rate over the dark control level, and the gene therefore appears to be of prime importance in the blue-light induction pathway ofN. crassa. We describe the sequencing and analysis ofbli-4 and the 38 kDa protein it encodes. We show that the protein is very rapidly imported into the mitochondria and exhibits high homology with the family of short-chain alcohol dehydrogenases.

Key words

Neurospora crassa Blue light Mitochondria Short-chain alcohol dehydrogenase 

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References

  1. Ahmad M, Cashmore AR (1993)HY4 gene ofA. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366:162–166CrossRefPubMedGoogle Scholar
  2. Bruchez JJP, Eberle J, Russo VEA (1993a) Regulatory sequences involved in the translation ofNeurospora crassa mRNA: Kozak sequences and stop codons. Fungal Genet Newslett 40:85–88Google Scholar
  3. Bruchez JJP, Eberle J, Russo VEA (1993b) Regulatory sequences in the transcription ofNeurospora crassa genes: CAAT box, TATA box, introns, poly(A) tail formation sequences. Fungal Genet Newslett 40:89–96Google Scholar
  4. Chen Z, Jiang JC, Lin Z-G, Lee WR, Baker ME, Chang SH (1993) Site-specific mutagenesis of Drosophila alcohol dehydrogenase: evidence for involvement of tyrosine-152 and lysine-156 in catalysis. Biochemistry 32:3342–3346CrossRefPubMedGoogle Scholar
  5. Chory J (1993) Out of darkness: mutants reveal pathways controlling light-regulated development in plants. Trends Genet 9:167–172CrossRefPubMedGoogle Scholar
  6. Corrochano LM, Lauter F-R, Ebbole DJ, Yanofsky C (1996) Light and developmental regulation of the genecon-10 ofNeurospora crassa. Proc Natl Acad Sci USA, in pressGoogle Scholar
  7. Cramer CL, Ristow JL, Paulus TJ, Davis RH (1983) Methods for mycelial breakage and isolation of mitochondria and vacuoles of Neurospora. Anal Biochem 128:384–392CrossRefPubMedGoogle Scholar
  8. Davis RH, deSerres FJ (1970) Genetic and microbiological research techniques forNeurospora crassa. Methods Enzymol 17A:79–143Google Scholar
  9. Degli-Innocenti F, Pohl U, Russo VEA (1983) Photoinduction of protoperithecia inNeurospora crassa by blue light. J Photochem Photobiol 37:49–51Google Scholar
  10. Degli-Innocenti F, Russo VEA (1984) Isolation of new White Collar mutants ofNeurospora crassa and studies on their behaviour in the blue-light induced formation of protoperithecia. J Bacteriol 159:757–761PubMedGoogle Scholar
  11. DeLong A, Calderon-Urrrea A, Dellaporta SL (1993) Sex determination geneT ASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 27:757–768CrossRefGoogle Scholar
  12. Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395PubMedGoogle Scholar
  13. Eberle J, Russo VEA (1992)Neurospora crassa blue-light-inducible genebli-7 encodes a short hydrophobic protein. DNA Sequence 3:131–141PubMedGoogle Scholar
  14. Eberle J, Russo VEA (1994)Neurospora crassa blue-light-inducible genebli-3. Biochem Molec Biol Int 34:737–744PubMedGoogle Scholar
  15. Fawcett TW, Barlett G (1990) An effective method for eliminating “artifact banding” when sequencing double-stranded DNA templates. Biotechniques 9:46–48PubMedGoogle Scholar
  16. Harding RW, Melles S (1983) Genetic analysis of phototropism ofNeurospora crassa perithecial beaks using White Collar and Albino mutants. Plant Physiol 72:996–1000Google Scholar
  17. Jornvall H, von Bahr-Lindstrom H, Jany KD, Ulmer W. Froschle M (1984) Extended superfamily of short alcohol-polyol-sugar dehydrogenases: structural similarities between glucose and ribitol dehydrogenases. FEBS Lett 165:190–196CrossRefPubMedGoogle Scholar
  18. Jungblut P, Eckerskorn C, Lottspeich F, Klose (1990) Blotting efficiency investigated by using two-dimensional electrophoresis, hydrophobic membranes and proteins from different sources. Electrophoresis 11:581–588CrossRefPubMedGoogle Scholar
  19. Kaldenhoff R, Russo VEA (1993) Promoter analysis of thebli-7/eas gene. Curr Genet 24:394–399CrossRefPubMedGoogle Scholar
  20. Kleene R, Pfanner N, Pfaller R, Link TA, Sebald W, Neupert W, Tropschung M (1987) Mitochondrial porin ofNeurospora crassa: cDNA cloning, in vitro expression and import into mitochondria. EMBO J 6:2627–2633PubMedGoogle Scholar
  21. Kohler W, Rensing L (1992) Light and the recovery from heat shock induce the synthesis of 38 kDa mitochondrial proteins inNeurospora crassa. Arch Microbiol 158:5–8CrossRefPubMedGoogle Scholar
  22. Kozak M (1987) An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res 15:8125–8148PubMedGoogle Scholar
  23. Krook M, Marekov L, Jornvall H (1990) Purification and structural characterization of placental NAD(+)-linked 15-hydroxyprostaglandir dehydrogenase. The primary structure reveals the enzyme to belong to the short-chain alcohol dehydrogenase family. Biochemistry 29:738–743CrossRefPubMedGoogle Scholar
  24. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefPubMedGoogle Scholar
  25. Lauter F-R, Russo VEA (1991) Blue light induction of conidiation-specific genes inNeurospora crassa. Nucleic Acids Res 19:6883–6886PubMedGoogle Scholar
  26. Lauter F-R, Russo VEA, Yanofsky C (1992) Development and light regulation ofeas, the structural gene for the rodlet protein of Neurospora. Genes Dev 6:2372–2381Google Scholar
  27. Lauter F-R, Yanofsky C (1993) Day/night and circadian rhythm control ofcon gene expression in Neurospora. Proc Natl Acad Sci USA 90:8249–8253PubMedGoogle Scholar
  28. Mandel M, Higa A (1970) Calcium-dependent bacteriophage DNA infection. J Mol Biol 53:159–162CrossRefPubMedGoogle Scholar
  29. Messing J (1983) New M13 vectors for cloning. Methods Enzymol 101:20–78PubMedGoogle Scholar
  30. Miyazaki K, Oshima T (1994) Tyr-139 inThermus thermophilus 3-isopropylmalate dehydrogenase is involved in catalytic function. FEBS Lett 332:37–38CrossRefGoogle Scholar
  31. Montague P (1987) Comparisons of the molecular structure between mammalian and lower eukaryotic genes. In: Kinghorn J (ed) Gene structure in eukaryotic microbes. IRL Press, Oxford, Washington DC, pp 263–285Google Scholar
  32. Nawrath C, Russo VEA (1990) Fast induction of translatable mRNA by blue light inNeurospora crassa wt: thewc-1 andwc-2 mutants are blind. J Photochem Photobiol B 4:261–271CrossRefPubMedGoogle Scholar
  33. Neidle E, Hartnett C, Ornston LN, Bairoch A, Rekik M, Harayama S (1992) Cis-diol dehydrogenases encoded by the TOL pWW0 plasmidxy/L gene and theAcinetobacter calcoaceticus chromosomalbenD gene are members of the short-chain alcohol dehydrogenase superfamily. Eur J Biochem 204:113–120CrossRefPubMedGoogle Scholar
  34. O'Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021PubMedGoogle Scholar
  35. Pietschmann S, Eberle J, Lauter F-R, Pandit NN, Russo VEA (1991) Co-regulation of two tandem genes by one blue-light element inNeurospora crassa. Fungal Genet Newslett 38:85–86Google Scholar
  36. Pohl U, Russo VEA (1984) Phototropism. In: Colombetti G, Lenci F (eds) Membranes and sensory transduction. Plenum Press, New York, London, pp 231–329Google Scholar
  37. Potapova TV, Levina NN, Belozerskaya TA, Kritskv MS, Chailakhian LM (1984) Investigation of electrophysiological responses ofNeurospora crassa to blue light. Arch Microbiol 137:262–265CrossRefGoogle Scholar
  38. Pugsley AP (1989) Protein targeting. Academic Press, San Diego, LondonGoogle Scholar
  39. Russo VEA (1988) Blue light induces circadian rhythms in thebd mutant of Neurospora: double mutantsbd, wc-1 andbd, wc-2 are blind. J Photochem Photobiol B 2:59–65CrossRefPubMedGoogle Scholar
  40. Sambrook J, Maniatis T, Fritsch EF (eds) (1989) Molecular cloning: a laboratory manual (2 edn) Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New YorkGoogle Scholar
  41. Sargent ML, Briggs WR (1967) The effects of light on a circadian rhythm of conidiation in Neurospora. Plant Physiol 42:1504–1510Google Scholar
  42. Schmidhauser TJ, Lauter F-R, Russo VEA, Yanofsky C (1990) Cloning, sequencing and photoregulation ofal-1, a carotenoid biosynthetic gene ofNeurospora crassa. Mol Cell Biol 10:5064–5070PubMedGoogle Scholar
  43. Schmidhauser TJ, Lauter F-R, Schumacher M, Zhou W, Russo VEA, Yanofsky C (1994) Characterization ofal-2, the phytoene synthase gene ofNeurospora crassa. J Biol Chem 269:12060–12066PubMedGoogle Scholar
  44. Schrott EL (1980) Dose response and related aspects to carotenogenesis inNeurospora crassa. In: Senger H (ed) The blue light syndrome. Springer-Verlag, Berlin-Heidelberg-New York, pp 309–320Google Scholar
  45. Sokolovsky V, Kaldenhoff R, Ricci M, Russo VEA (1990) Fast and reliable mini-prep RNA extraction fromNeurospora crassa. Fungal Genet Newslett 37:41–43Google Scholar
  46. Sommer T (1988) Ph.D. Thesis, Freie Universität BerlinGoogle Scholar
  47. Sommer T, Chambers JAA, Eberle J, Lauter F-R Russo VEA (1989) Fast light-regulated genes ofNeurospora crassa. Nucleic Acids Res 17:5713–5723PubMedGoogle Scholar
  48. Von Heijne G (1986) Mitochondrial targeting sequences may form amphiphilic helices. EMBO J 5:1335–1342PubMedGoogle Scholar
  49. White BT, Yanofsky C (1993) Structural characterization and expression analysis of the Neurospora conidiation genecon-6. Dev Biol 160:254–264CrossRefPubMedGoogle Scholar
  50. White WB, Franklund CV, Coleman JP, Hylemon PB (1988) Evidence for a multigene family involved in bile acid 7-hydroxylation inEubacterium sp. strain VPI 12708. J Bacteriol 170:4555–4561PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • J. J. P. Bruchez
    • 1
  • J. Eberle
    • 1
  • W. Kohler
    • 1
  • V. Kruft
    • 1
  • A. Radford
    • 1
  • V. E. A. Russo
    • 1
  1. 1.Max-Planck-Institut für molekulare GenetikBerlinGermany

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