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Nucleic Acids Res. Dec 11, 1991; 19(23): 6511–6517.
PMCID: PMC329209

Coordinate expression of ribosomal protein genes in Neurospora crassa and identification of conserved upstream sequences.

Abstract

The relative levels of rRNAs and ribosomal proteins are coordinately regulated by growth rate and carbon nutrition in Neurospora crassa. However, little is known about the mechanisms involved. To investigate the transcriptional regulation of ribosomal protein genes in N. crassa, we cloned and sequenced a ribosomal protein gene (crp-3). The inferred crp-3 protein sequence shares 89% and 83% homology at its N-terminus with the yeast rp51 and the human S17 ribosomal proteins respectively. The crp-3 gene contains two introns, neither of which are conserved in position with the RP51 or the S17 genes. The crp-3 gene is present in a single copy and was mapped by RFLP analysis to the right arm of linkage group IV, near the cot-1 locus. Sequence comparisons of the upstream regions of the three sequenced crp genes revealed several common features. These include a 'Taq box' (consensus: ARTTYGACTT) at -39, a CG repeat (consensus: CCCRCCRRR) at -65, and a major transcription initiation site embedded in a purine rich region flanked by an upstream pyrimidine rich sequence. Using four N.crassa ribosomal protein genes as probes, we demonstrated that the levels of the four ribosomal protein mRNAs were closely coordinated during a nutritional downshift from sucrose to quinic acid.

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Selected References

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  • Kief DR, Warner JR. Coordinate control of syntheses of ribosomal ribonucleic acid and ribosomal proteins during nutritional shift-up in Saccharomyces cerevisiae. Mol Cell Biol. 1981 Nov;1(11):1007–1015. [PMC free article] [PubMed]
  • Mager WH. Control of ribosomal protein gene expression. Biochim Biophys Acta. 1988 Jan 25;949(1):1–15. [PubMed]
  • Alberghina L, Sturani E. Control of growth and of the nuclear division cycle in Neurospora crassa. Microbiol Rev. 1981 Mar;45(1):99–122. [PMC free article] [PubMed]
  • Nomura M, Gourse R, Baughman G. Regulation of the synthesis of ribosomes and ribosomal components. Annu Rev Biochem. 1984;53:75–117. [PubMed]
  • Warner JR. Synthesis of ribosomes in Saccharomyces cerevisiae. Microbiol Rev. 1989 Jun;53(2):256–271. [PMC free article] [PubMed]
  • Warner JR, Gorenstein C. The synthesis of eucaryotic ribosomal proteins in vitro. Cell. 1977 May;11(1):201–212. [PubMed]
  • Warner JR, Gorenstein C. Yeast has a true stringent response. Nature. 1978 Sep 28;275(5678):338–339. [PubMed]
  • Warner JR, Mitra G, Schwindinger WF, Studeny M, Fried HM. Saccharomyces cerevisiae coordinates accumulation of yeast ribosomal proteins by modulating mRNA splicing, translational initiation, and protein turnover. Mol Cell Biol. 1985 Jun;5(6):1512–1521. [PMC free article] [PubMed]
  • Pearson NJ, Haber JE. Changes in regulation of ribosomal protein synthesis during vegetative growth and sporulation of Saccharomyces cerevisiae. J Bacteriol. 1980 Sep;143(3):1411–1419. [PMC free article] [PubMed]
  • Kraig E, Haber JE, Rosbash M. Sporulation and rna2 lower ribosomal protein mRNA levels by different mechanisms in Saccharomyces cerevisiae. Mol Cell Biol. 1982 Oct;2(10):1199–1204. [PMC free article] [PubMed]
  • Planta RJ, Raué HA. Control of ribosome biogenesis in yeast. Trends Genet. 1988 Mar;4(3):64–68. [PubMed]
  • Teem JL, Abovich N, Kaufer NF, Schwindinger WF, Warner JR, Levy A, Woolford J, Leer RJ, van Raamsdonk-Duin MM, Mager WH, et al. A comparison of yeast ribosomal protein gene DNA sequences. Nucleic Acids Res. 1984 Nov 26;12(22):8295–8312. [PMC free article] [PubMed]
  • Donovan DM, Pearson NJ. Transcriptional regulation of ribosomal proteins during a nutritional upshift in Saccharomyces cerevisiae. Mol Cell Biol. 1986 Jul;6(7):2429–2435. [PMC free article] [PubMed]
  • Rotenberg MO, Woolford JL., Jr Tripartite upstream promoter element essential for expression of Saccharomyces cerevisiae ribosomal protein genes. Mol Cell Biol. 1986 Feb;6(2):674–687. [PMC free article] [PubMed]
  • Herruer MH, Mager WH, Woudt LP, Nieuwint RT, Wassenaar GM, Groeneveld P, Planta RJ. Transcriptional control of yeast ribosomal protein synthesis during carbon-source upshift. Nucleic Acids Res. 1987 Dec 23;15(24):10133–10144. [PMC free article] [PubMed]
  • Mann C, Buhler JM, Treich I, Sentenac A. RPC40, a unique gene for a subunit shared between yeast RNA polymerases A and C. Cell. 1987 Feb 27;48(4):627–637. [PubMed]
  • Buchman AR, Kimmerly WJ, Rine J, Kornberg RD. Two DNA-binding factors recognize specific sequences at silencers, upstream activating sequences, autonomously replicating sequences, and telomeres in Saccharomyces cerevisiae. Mol Cell Biol. 1988 Jan;8(1):210–225. [PMC free article] [PubMed]
  • Buchman AR, Lue NF, Kornberg RD. Connections between transcriptional activators, silencers, and telomeres as revealed by functional analysis of a yeast DNA-binding protein. Mol Cell Biol. 1988 Dec;8(12):5086–5099. [PMC free article] [PubMed]
  • Huet J, Sentenac A. TUF, the yeast DNA-binding factor specific for UASrpg upstream activating sequences: identification of the protein and its DNA-binding domain. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3648–3652. [PMC free article] [PubMed]
  • Shore D, Stillman DJ, Brand AH, Nasmyth KA. Identification of silencer binding proteins from yeast: possible roles in SIR control and DNA replication. EMBO J. 1987 Feb;6(2):461–467. [PMC free article] [PubMed]
  • Shore D, Nasmyth K. Purification and cloning of a DNA binding protein from yeast that binds to both silencer and activator elements. Cell. 1987 Dec 4;51(5):721–732. [PubMed]
  • Wittekind M, Kolb JM, Dodd J, Yamagishi M, Mémet S, Buhler JM, Nomura M. Conditional expression of RPA190, the gene encoding the largest subunit of yeast RNA polymerase I: effects of decreased rRNA synthesis on ribosomal protein synthesis. Mol Cell Biol. 1990 May;10(5):2049–2059. [PMC free article] [PubMed]
  • Dudov KP, Perry RP. Properties of a mouse ribosomal protein promoter. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8545–8549. [PMC free article] [PubMed]
  • Hariharan N, Kelley DE, Perry RP. Equipotent mouse ribosomal protein promoters have a similar architecture that includes internal sequence elements. Genes Dev. 1989 Nov;3(11):1789–1800. [PubMed]
  • Hariharan N, Perry RP. A characterization of the elements comprising the promoter of the mouse ribosomal protein gene RPS16. Nucleic Acids Res. 1989 Jul 11;17(13):5323–5337. [PMC free article] [PubMed]
  • Hariharan N, Perry RP. Functional dissection of a mouse ribosomal protein promoter: significance of the polypyrimidine initiator and an element in the TATA-box region. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1526–1530. [PMC free article] [PubMed]
  • Meyuhas O, Klein A. The mouse ribosomal protein L7 gene. Its primary structure and functional analysis of the promoter region. J Biol Chem. 1990 Jul 15;265(20):11465–11473. [PubMed]
  • Schmidt T, Chen PS, Pellegrini M. The induction of ribosome biosynthesis in a nonmitotic secretory tissue. J Biol Chem. 1985 Jun 25;260(12):7645–7650. [PubMed]
  • Kay MA, Jacobs-Lorena M. Selective translational regulation of ribosomal protein gene expression during early development of Drosophila melanogaster. Mol Cell Biol. 1985 Dec;5(12):3583–3592. [PMC free article] [PubMed]
  • Pierandrei-Amaldi P, Campioni N, Gallinari P, Beccari E, Bozzoni I, Amaldi F. Ribosomal-protein synthesis is not autogenously regulated at the translational level in Xenopus laevis. Dev Biol. 1985 Feb;107(2):281–289. [PubMed]
  • Mariottini P, Amaldi F. The 5' untranslated region of mRNA for ribosomal protein S19 is involved in its translational regulation during Xenopus development. Mol Cell Biol. 1990 Feb;10(2):816–822. [PMC free article] [PubMed]
  • Meyuhas O, Thompson EA, Jr, Perry RP. Glucocorticoids selectively inhibit translation of ribosomal protein mRNAs in P1798 lymphosarcoma cells. Mol Cell Biol. 1987 Aug;7(8):2691–2699. [PMC free article] [PubMed]
  • Sturani E, Magnani F, Alberghina FA. Inhibition of ribosomal RNA synthesis during a shift-down transition of growth in Neurospora crassa. Biochim Biophys Acta. 1973 Aug 24;319(2):153–164. [PubMed]
  • Alberghina FA, Sturani E, Gohlke JR. Levels and rates of synthesis of ribosomal ribonucleic acid, transfer ribonucleic acid, and protein in Neurospora crassa in different steady states of growth. J Biol Chem. 1975 Jun 25;250(12):4381–4388. [PubMed]
  • Tyler BM. Transcription of Neurospora crassa 5 S rRNA genes requires a TATA box and three internal elements. J Mol Biol. 1987 Aug 20;196(4):801–811. [PubMed]
  • Tyler BM. Two complex regions, including a TATA sequence, are required for transcription by RNA polymerase I in Neurospora crassa. Nucleic Acids Res. 1990 Apr 11;18(7):1805–1811. [PMC free article] [PubMed]
  • Shi YG, Tyler BM. All internal promoter elements of Neurospora crassa 5 S rRNA and tRNA genes, including the A boxes, are functionally gene-specific. J Biol Chem. 1991 May 5;266(13):8015–8019. [PubMed]
  • Tyler BM, Harrison K. A Neurospora crassa ribosomal protein gene, homologous to yeast CRY1, contains sequences potentially coordinating its transcription with rRNA genes. Nucleic Acids Res. 1990 Oct 11;18(19):5759–5765. [PMC free article] [PubMed]
  • Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. [PubMed]
  • Short JM, Fernandez JM, Sorge JA, Huse WD. Lambda ZAP: a bacteriophage lambda expression vector with in vivo excision properties. Nucleic Acids Res. 1988 Aug 11;16(15):7583–7600. [PMC free article] [PubMed]
  • Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. [PubMed]
  • Maxam AM, Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. [PubMed]
  • Shi YG, Tyler BM. Pyrrolidine, a non-controlled substance, can replace piperidine for the chemical sequencing of DNA. Nucleic Acids Res. 1989 Apr 25;17(8):3317–3317. [PMC free article] [PubMed]
  • Metzenberg RL, Stevens JN, Selker EU, Morzycka-Wroblewska E. Identification and chromosomal distribution of 5S rRNA genes in Neurospora crassa. Proc Natl Acad Sci U S A. 1985 Apr;82(7):2067–2071. [PMC free article] [PubMed]
  • Giles NH, Case ME, Baum J, Geever R, Huiet L, Patel V, Tyler B. Gene organization and regulation in the qa (quinic acid) gene cluster of Neurospora crassa. Microbiol Rev. 1985 Sep;49(3):338–358. [PMC free article] [PubMed]
  • Patel VB, Schweizer M, Dykstra CC, Kushner SR, Giles NH. Genetic organization and transcriptional regulation in the qa gene cluster of Neurospora crassa. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5783–5787. [PMC free article] [PubMed]
  • Kreader CA, Heckman JE. Isolation and characterization of a Neurospora crassa ribosomal protein gene homologous to CYH2 of yeast. Nucleic Acids Res. 1987 Nov 11;15(21):9027–9042. [PMC free article] [PubMed]
  • Orbach MJ, Porro EB, Yanofsky C. Cloning and characterization of the gene for beta-tubulin from a benomyl-resistant mutant of Neurospora crassa and its use as a dominant selectable marker. Mol Cell Biol. 1986 Jul;6(7):2452–2461. [PMC free article] [PubMed]
  • Chen IT, Dixit A, Rhoads DD, Roufa DJ. Homologous ribosomal proteins in bacteria, yeast, and humans. Proc Natl Acad Sci U S A. 1986 Sep;83(18):6907–6911. [PMC free article] [PubMed]
  • Rambosek J, Leach J. Recombinant DNA in filamentous fungi: progress and prospects. Crit Rev Biotechnol. 1987;6(4):357–393. [PubMed]
  • Tyler BM, Geever RF, Case ME, Giles NH. Cis-acting and trans-acting regulatory mutations define two types of promoters controlled by the qa-1F gene of Neurospora. Cell. 1984 Feb;36(2):493–502. [PubMed]
  • Struhl K. Molecular mechanisms of transcriptional regulation in yeast. Annu Rev Biochem. 1989;58:1051–1077. [PubMed]
  • Teem JL, Rosbash M. Expression of a beta-galactosidase gene containing the ribosomal protein 51 intron is sensitive to the rna2 mutation of yeast. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4403–4407. [PMC free article] [PubMed]
  • Chen IT, Roufa DJ. The transcriptionally active human ribosomal protein S17 gene. Gene. 1988 Oct 15;70(1):107–116. [PubMed]
  • Geever RF, Huiet L, Baum JA, Tyler BM, Patel VB, Rutledge BJ, Case ME, Giles NH. DNA sequence, organization and regulation of the qa gene cluster of Neurospora crassa. J Mol Biol. 1989 May 5;207(1):15–34. [PubMed]
  • Tarawneh KA, Wang Z, Free SJ. Nucleotide sequence of a Neurospora crassa ribosomal protein gene. Nucleic Acids Res. 1990 Dec 25;18(24):7445–7445. [PMC free article] [PubMed]
  • Woudt LP, Smit AB, Mager WH, Planta RJ. Conserved sequence elements upstream of the gene encoding yeast ribosomal protein L25 are involved in transcription activation. EMBO J. 1986 May;5(5):1037–1040. [PMC free article] [PubMed]
  • Larkin JC, Thompson JR, Woolford JL., Jr Structure and expression of the Saccharomyces cerevisiae CRY1 gene: a highly conserved ribosomal protein gene. Mol Cell Biol. 1987 May;7(5):1764–1775. [PMC free article] [PubMed]
  • Schwindinger WF, Warner JR. Transcriptional elements of the yeast ribosomal protein gene CYH2. J Biol Chem. 1987 Apr 25;262(12):5690–5695. [PubMed]
  • Dynan WS, Tjian R. Control of eukaryotic messenger RNA synthesis by sequence-specific DNA-binding proteins. Nature. 316(6031):774–778. [PubMed]
  • Courey AJ, Holtzman DA, Jackson SP, Tjian R. Synergistic activation by the glutamine-rich domains of human transcription factor Sp1. Cell. 1989 Dec 1;59(5):827–836. [PubMed]
  • Hamer JE, Timberlake WE. Functional organization of the Aspergillus nidulans trpC promoter. Mol Cell Biol. 1987 Jul;7(7):2352–2359. [PMC free article] [PubMed]
  • Punt PJ, Dingemanse MA, Kuyvenhoven A, Soede RD, Pouwels PH, van den Hondel CA. Functional elements in the promoter region of the Aspergillus nidulans gpdA gene encoding glyceraldehyde-3-phosphate dehydrogenase. Gene. 1990 Sep 1;93(1):101–109. [PubMed]
  • Ballance DJ. Sequences important for gene expression in filamentous fungi. Yeast. 1986 Dec;2(4):229–236. [PubMed]
  • Sturani E, Costantini MG, Zippel R, Alberghina FA. Regulation of RNA synthesis in Neurospora crassa. An analysis of a shift-up. Exp Cell Res. 1976 May;99(2):245–252. [PubMed]

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