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Mol Cell Biol. May 1994; 14(5): 2905–2913.
PMCID: PMC358658

Suppression of yeast RNA polymerase III mutations by FHL1, a gene coding for a fork head protein involved in rRNA processing.

Abstract

The FHL1 gene was isolated by screening for high-copy-number suppressors of conditional RNA polymerase III mutations. This gene is unique on the yeast genome and was located close to RPC40 and PRE2 on the right arm of chromosome XVI. It codes for a 936-amino-acid protein containing a domain similar to the fork head DNA-binding domain, initially found in the developmental fork head protein of Drosophila melanogaster and in the HNF-3 family of hepatocyte mammalian transcription factors. Null mutations caused a severe reduction in growth rate and a lower rRNA content that resulted from defective rRNA processing. There was no detectable effect on mRNA splicing. Thus, the Fhl1p protein plays a key role in the control of rRNA processing, presumably by acting as a transcriptional regulator of genes specifically involved in that process. Moreover, mutants carrying the RNA polymerase III mutations were slightly defective in rRNA processing. This accounts for the isolation of FHL1 as a dosage-dependent suppressor and suggests that rRNA processing depends on a still-unidentified RNA polymerase III transcript.

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  • Allison LA, Ingles CJ. Mutations in RNA polymerase II enhance or suppress mutations in GAL4. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2794–2798. [PMC free article] [PubMed]
  • Allison LA, Moyle M, Shales M, Ingles CJ. Extensive homology among the largest subunits of eukaryotic and prokaryotic RNA polymerases. Cell. 1985 Sep;42(2):599–610. [PubMed]
  • Beltrame M, Tollervey D. Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA. EMBO J. 1992 Apr;11(4):1531–1542. [PMC free article] [PubMed]
  • Boeke JD, LaCroute F, Fink GR. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet. 1984;197(2):345–346. [PubMed]
  • Bogenhagen DF, Brown DD. Nucleotide sequences in Xenopus 5S DNA required for transcription termination. Cell. 1981 Apr;24(1):261–270. [PubMed]
  • Chapon C, Legrain P. A novel gene, spp91-1, suppresses the splicing defect and the pre-mRNA nuclear export in the prp9-1 mutant. EMBO J. 1992 Sep;11(9):3279–3288. [PMC free article] [PubMed]
  • Chiannilkulchai N, Stalder R, Riva M, Carles C, Werner M, Sentenac A. RPC82 encodes the highly conserved, third-largest subunit of RNA polymerase C (III) from Saccharomyces cerevisiae. Mol Cell Biol. 1992 Oct;12(10):4433–4440. [PMC free article] [PubMed]
  • Clark KL, Halay ED, Lai E, Burley SK. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature. 1993 Jul 29;364(6436):412–420. [PubMed]
  • Della Seta F, Treich I, Buhler JM, Sentenac A. ABF1 binding sites in yeast RNA polymerase genes. J Biol Chem. 1990 Sep 5;265(25):15168–15175. [PubMed]
  • Dequard-Chablat M, Riva M, Carles C, Sentenac A. RPC19, the gene for a subunit common to yeast RNA polymerases A (I) and C (III). J Biol Chem. 1991 Aug 15;266(23):15300–15307. [PubMed]
  • Dirksen ML, Jamrich M. A novel, activin-inducible, blastopore lip-specific gene of Xenopus laevis contains a fork head DNA-binding domain. Genes Dev. 1992 Apr;6(4):599–608. [PubMed]
  • Gabrielsen OS, Sentenac A. RNA polymerase III (C) and its transcription factors. Trends Biochem Sci. 1991 Nov;16(11):412–416. [PubMed]
  • Geiduschek EP, Tocchini-Valentini GP. Transcription by RNA polymerase III. Annu Rev Biochem. 1988;57:873–914. [PubMed]
  • Gudenus R, Mariotte S, Moenne A, Ruet A, Memet S, Buhler JM, Sentenac A, Thuriaux P. Conditional mutants of RPC160, the gene encoding the largest subunit of RNA polymerase C in Saccharomyces cerevisiae. Genetics. 1988 Jul;119(3):517–526. [PMC free article] [PubMed]
  • Heinemeyer W, Gruhler A, Möhrle V, Mahé Y, Wolf DH. PRE2, highly homologous to the human major histocompatibility complex-linked RING10 gene, codes for a yeast proteasome subunit necessary for chrymotryptic activity and degradation of ubiquitinated proteins. J Biol Chem. 1993 Mar 5;268(7):5115–5120. [PubMed]
  • Hoffman CS, Winston F. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene. 1987;57(2-3):267–272. [PubMed]
  • Huet J, Riva M, Sentenac A, Fromageot P. Yeast RNA polymerase C and its subunits. Specific antibodies as structural and functional probes. J Biol Chem. 1985 Dec 5;260(28):15304–15310. [PubMed]
  • Hughes JM, Konings DA, Cesareni G. The yeast homologue of U3 snRNA. EMBO J. 1987 Jul;6(7):2145–2155. [PMC free article] [PubMed]
  • James P, Hall BD. ret1-1, a yeast mutant affecting transcription termination by RNA polymerase III. Genetics. 1990 Jun;125(2):293–303. [PMC free article] [PubMed]
  • Kiss T, Marshallsay C, Filipowicz W. Alteration of the RNA polymerase specificity of U3 snRNA genes during evolution and in vitro. Cell. 1991 May 3;65(3):517–526. [PubMed]
  • Kiss T, Marshallsay C, Filipowicz W. 7-2/MRP RNAs in plant and mammalian cells: association with higher order structures in the nucleolus. EMBO J. 1992 Oct;11(10):3737–3746. [PMC free article] [PubMed]
  • Köhrer K, Domdey H. Preparation of high molecular weight RNA. Methods Enzymol. 1991;194:398–405. [PubMed]
  • Lai E, Prezioso VR, Smith E, Litvin O, Costa RH, Darnell JE., Jr HNF-3A, a hepatocyte-enriched transcription factor of novel structure is regulated transcriptionally. Genes Dev. 1990 Aug;4(8):1427–1436. [PubMed]
  • Lai E, Prezioso VR, Tao WF, Chen WS, Darnell JE., Jr Hepatocyte nuclear factor 3 alpha belongs to a gene family in mammals that is homologous to the Drosophila homeotic gene fork head. Genes Dev. 1991 Mar;5(3):416–427. [PubMed]
  • Lalo D, Carles C, Sentenac A, Thuriaux P. Interactions between three common subunits of yeast RNA polymerases I and III. Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5524–5528. [PMC free article] [PubMed]
  • Laughon A, Gesteland RF. Isolation and preliminary characterization of the GAL4 gene, a positive regulator of transcription in yeast. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6827–6831. [PMC free article] [PubMed]
  • Legrain P, Rosbash M. Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm. Cell. 1989 May 19;57(4):573–583. [PubMed]
  • Li C, Lai CF, Sigman DS, Gaynor RB. Cloning of a cellular factor, interleukin binding factor, that binds to NFAT-like motifs in the human immunodeficiency virus long terminal repeat. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7739–7743. [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]
  • Mann C, Micouin JY, Chiannilkulchai N, Treich I, Buhler JM, Sentenac A. RPC53 encodes a subunit of Saccharomyces cerevisiae RNA polymerase C (III) whose inactivation leads to a predominantly G1 arrest. Mol Cell Biol. 1992 Oct;12(10):4314–4326. [PMC free article] [PubMed]
  • Marck C. 'DNA Strider': a 'C' program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers. Nucleic Acids Res. 1988 Mar 11;16(5):1829–1836. [PMC free article] [PubMed]
  • Mémet S, Saurin W, Sentenac A. RNA polymerases B and C are more closely related to each other than to RNA polymerase A. J Biol Chem. 1988 Jul 25;263(21):10048–10051. [PubMed]
  • Miller LM, Gallegos ME, Morisseau BA, Kim SK. lin-31, a Caenorhabditis elegans HNF-3/fork head transcription factor homolog, specifies three alternative cell fates in vulval development. Genes Dev. 1993 Jun;7(6):933–947. [PubMed]
  • Moenne A, Camier S, Anderson G, Margottin F, Beggs J, Sentenac A. The U6 gene of Saccharomyces cerevisiae is transcribed by RNA polymerase C (III) in vivo and in vitro. EMBO J. 1990 Jan;9(1):271–277. [PMC free article] [PubMed]
  • Mosrin C, Riva M, Beltrame M, Cassar E, Sentenac A, Thuriaux P. The RPC31 gene of Saccharomyces cerevisiae encodes a subunit of RNA polymerase C (III) with an acidic tail. Mol Cell Biol. 1990 Sep;10(9):4737–4743. [PMC free article] [PubMed]
  • Nonet M, Scafe C, Sexton J, Young R. Eucaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis. Mol Cell Biol. 1987 May;7(5):1602–1611. [PMC free article] [PubMed]
  • Orr-Weaver TL, Szostak JW, Rothstein RJ. Yeast transformation: a model system for the study of recombination. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6354–6358. [PMC free article] [PubMed]
  • Parikh VS, Conrad-Webb H, Docherty R, Butow RA. Interaction between the yeast mitochondrial and nuclear genomes influences the abundance of novel transcripts derived from the spacer region of the nuclear ribosomal DNA repeat. Mol Cell Biol. 1989 May;9(5):1897–1907. [PMC free article] [PubMed]
  • Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. [PMC free article] [PubMed]
  • Russell ID, Tollervey D. NOP3 is an essential yeast protein which is required for pre-rRNA processing. J Cell Biol. 1992 Nov;119(4):737–747. [PMC free article] [PubMed]
  • Sachs AB, Davis RW. Translation initiation and ribosomal biogenesis: involvement of a putative rRNA helicase and RPL46. Science. 1990 Mar 2;247(4946):1077–1079. [PubMed]
  • Schmitt ME, Brown TA, Trumpower BL. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res. 1990 May 25;18(10):3091–3092. [PMC free article] [PubMed]
  • Schmitt ME, Clayton DA. Yeast site-specific ribonucleoprotein endoribonuclease MRP contains an RNA component homologous to mammalian RNase MRP RNA and essential for cell viability. Genes Dev. 1992 Oct;6(10):1975–1985. [PubMed]
  • Sherman F. Getting started with yeast. Methods Enzymol. 1991;194:3–21. [PubMed]
  • Stettler S, Chiannilkulchai N, Hermann-Le Denmat S, Lalo D, Lacroute F, Sentenac A, Thuriaux P. A general suppressor of RNA polymerase I, II and III mutations in Saccharomyces cerevisiae. Mol Gen Genet. 1993 May;239(1-2):169–176. [PubMed]
  • Stettler S, Mariotte S, Riva M, Sentenac A, Thuriaux P. An essential and specific subunit of RNA polymerase III (C) is encoded by gene RPC34 in Saccharomyces cerevisiae. J Biol Chem. 1992 Oct 25;267(30):21390–21395. [PubMed]
  • Tao W, Lai E. Telencephalon-restricted expression of BF-1, a new member of the HNF-3/fork head gene family, in the developing rat brain. Neuron. 1992 May;8(5):957–966. [PubMed]
  • Tollervey D, Lehtonen H, Carmo-Fonseca M, Hurt EC. The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing in yeast. EMBO J. 1991 Mar;10(3):573–583. [PMC free article] [PubMed]
  • Treich I, Carles C, Riva M, Sentenac A. RPC10 encodes a new mini subunit shared by yeast nuclear RNA polymerases. Gene Expr. 1992;2(1):31–37. [PubMed]
  • Warner JR, Udem SA. Temperature sensitive mutations affecting ribosome synthesis in Saccharomyces cerevisiae. J Mol Biol. 1972 Mar 28;65(2):243–257. [PubMed]
  • Weigel D, Jäckle H. The fork head domain: a novel DNA binding motif of eukaryotic transcription factors? Cell. 1990 Nov 2;63(3):455–456. [PubMed]
  • Weigel D, Jürgens G, Küttner F, Seifert E, Jäckle H. The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell. 1989 May 19;57(4):645–658. [PubMed]
  • Werner M, Chaussivert N, Willis IM, Sentenac A. Interaction between a complex of RNA polymerase III subunits and the 70-kDa component of transcription factor IIIB. J Biol Chem. 1993 Oct 5;268(28):20721–20724. [PubMed]
  • Werner M, Hermann-Le Denmat S, Treich I, Sentenac A, Thuriaux P. Effect of mutations in a zinc-binding domain of yeast RNA polymerase C (III) on enzyme function and subunit association. Mol Cell Biol. 1992 Mar;12(3):1087–1095. [PMC free article] [PubMed]
  • Wittekind M, Dodd J, Vu L, Kolb JM, Buhler JM, Sentenac A, Nomura M. Isolation and characterization of temperature-sensitive mutations in RPA190, the gene encoding the largest subunit of RNA polymerase I from Saccharomyces cerevisiae. Mol Cell Biol. 1988 Oct;8(10):3997–4008. [PMC free article] [PubMed]
  • Woychik NA, Liao SM, Kolodziej PA, Young RA. Subunits shared by eukaryotic nuclear RNA polymerases. Genes Dev. 1990 Mar;4(3):313–323. [PubMed]
  • Zhu G, Muller EG, Amacher SL, Northrop JL, Davis TN. A dosage-dependent suppressor of a temperature-sensitive calmodulin mutant encodes a protein related to the fork head family of DNA-binding proteins. Mol Cell Biol. 1993 Mar;13(3):1779–1787. [PMC free article] [PubMed]

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