Abstract
The rate of ribosomal protein gene (rp-gene) transcription in yeast is accurately adjusted to the cellular requirement for ribosomes under various growth conditions. However, the molecular mechanisms underlying this co-ordinated transcriptional control have not yet been elucidated. Transcriptional activation of rp-genes is mediated through two different multifunctional trans-acting factors, ABF1 and RAP1. In this report, we demonstrate that changes in cellular rp-mRNA levels during varying growth conditions are not parallelled by changes in the in vitro binding capacity of ABF1 or RAP1 for their cognate sequences. In addition, the nutritional upshift response of rp-genes observed after addition of glucose to a culture growing on a non-fermentative carbon source turns out not to be the result of increased expression of the ABF1 and RAP1 genes or of elevated DNA-binding activity of these factors. Therefore, growth rate-dependent transcription regulation of rp-genes is most probably not mediated by changes in the efficiency of binding of ABF1 and RAP1 to the upstream activation sites of these genes, but rather through other alterations in the efficiency of transcription activation. Furthermore, we tested the possibility that cAMP may play a role in elevating rp-gene expression during a nutritional shift-up. We found that the nutritional upshift response occurs normally in several mutants defective in cAMP metabolism.
Access this article
We’re sorry, something doesn't seem to be working properly.
Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.
Similar content being viewed by others
References
Becher dos Passos J, Vanhalewyn M, Brandao R, Castro I, Nicoli J, Thevelein J (1992) Glucose-induced activation of plasma membrane H+-ATPase in mutants of the yeast Saccharomyces cerevisiae affected in cAMP metabolism, CAMP-dependent protein phosphorylation and the initiation of glycolysis. Biochim Biophys Acta 1136:57–67
Berman J, Tachinaba C, Tye B (1986) Identification of a telomerebinding activity from yeast. Proc Natl Acad Sci USA 83:3713–3717
Beullens M, Mbonyi K, Geerts L, Gladines D, Detremrie K, Jans A, Thevelein J (1988) Studies on the mechanism of the glucose-induced cAMP signal in glycolysis and glucose repression mutants of the yeast Saccharomyces cerevisiae. Eur J Biochem 172:227–231
Boutelet F, Petitjean A, Hilger F (1985) Yeast cdc35 mutants are defective in adenylate cyclase and are allelic with cyr1 mutants while CAS1, a new gene, is involved in the regulation of adenylate cyclase. EMBO J 4:2635–2641
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brand A, Micklen H, Nasmyth K (1987) A yeast silencer contains sequences that can promote autonomous plasmid replication and transcriptional activation. Cell 51:709–719
Broach J (1991) RAS genes in Saccharomyces cerevisiae: signal transduction in search of a pathway. Trends Genet 7:28–33
Bromley S, Hereford L, Rosbash M (1982) Further evidence that the rna2 mutation of Saccharomyces cerevisiae affects mRNA processing. Mol Cell Biol 2:1205–1211
Buchman AR, Kimmerly WJ, Rine J, Kornberg RD (1988a) Two DNA-binding factors recognize specific sequences at silencers, upstream activating sequences, autonomously replicating sequences and telomeres in Saccharomyces cerevisiae. Mol Cell Biol 8:210–225
Buchman AR, Lue N, Kornberg RD (1988b) Connections between transcriptional activators, silencers and telomeres as revealed by functional analysis of a yeast DNA-binding protein. Mol Cell Biol 8:5086–5099
Chambers A, Tsang J, Stanway C, Kingsman A, Kingsman S (1989) Transcriptional control of the Saccharomyces cerevisiae PGK gene by RAP1. Mol Cell Biol 9:5517–5524
Chambers A, Stanway J, Tsang Y, Henry A, Kingsman A, Kingsman S (1990) ARS binding factor 1 binds adjacent to RAP1 at the UASs of the yeast glycolysis genes PGK and PYK1. Nucleic Acids Res 18:5393–5399
Diffley JFX, Stillman B (1989) Similarity between the transcriptional silencer binding proteins ABF1 and RAP1. Science 246:1034–1038
Doorenbosch MM, Mager WH, Planta RJ (1992) Multifunctional DNA-binding proteins in yeast. Gene Expression 2:193–201
Dorsman JC, Doorenbosch MM, Maurer CT, de Winde JH, Mager WH, Planta RJ, Grivell LA (1989) An ARS/silencer binding factor also activates two ribosomal protein genes in yeast. Nucleic Acids Res 17:4917–4923
Francesconi SC, Eisenberg S (1991) The multifunctional protein OBF1 is phosphorylated at serine and threonine residues in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 88:4089–4093
Francois J, Van Schaftingen E, Hers H (1984) The mechanism by which glucose increases fructose 2,6-biphosphate concentration in Saccharomyces cerevisiae. Eur J Biochem 145:187–193
Gallwitz D, Sures I (1980) Structure of a split yeast gene: complete nucleotide sequence of the actin gene in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 77:2546–2550
Gonçalves P, Maurer K, Mager WH, Planta RJ (1992) Kluyveromyces contains a functional ABF1-homologue. Nucleic Acids Res 20:2211–2215
Halfter H, Kavety B, Vandekerckhove H, Kiefer F, Gallwitz D (1989) Sequence, expression and mutational analysis of BAF1, a transcriptional activator and ARS1-binding protein of the yeast Saccharomyces cerevisiae. EMBO J 8:4265–4272
Hamil KG, Nam HG, Fried HM (1988) Constitutive transcription of yeast ribosomal protein gene TCM1 is promoted by uncommon cis- and trans-acting elements. Mol Cell Biol 8:4328–4341
Hardy C, Balderes D, Shore D (1992) Dissection of a carboxyterminal region of the yeast regulatory protein RAP1 with effects on both transcriptional activation and silencing. Mol Cell Biol 12:1209–1217
Henry Y, Chambers J, Tsang J, Kingsman A, Kingsman S (1990) Characterisation of the DNA binding domain of the yeast RAP1 protein. Nucleic Acids Res 18:2617–2623
Hofmann J, Laroche T, Brand G, Gasser S (1989) RAP-1 factor is necessary for DNA loop formation in vitro at the silent mating type locus HML. Cell 57:725–737
Huet J, Cottrelle P, Cool M, Vignais M, Thiele E, Marck C, Buhler J, Sentenac A, Fromageot P (1985) A general upstream binding factor for genes of the yeast translational apparatus. EMBO J 4:3539–3547
Kraakman LS, Mager WH, Grootjans J, Planta RJ (1991) Functional analysis of the promoter of the gene encoding the acidic ribosomal protein L45 in yeast. Biochim Biophys Acta 1090:204–210
Leer R, Van Raamsdonk-Duin M, Schoppink P, Cornelissen M, Cohen L, Mager WH, Planta RJ (1983) Yeast ribosomal protein S33 is encoded by an unsplit gene. Nucleic Acids Res 11:7759–7768
Leer R, van Raamsdonk-Duin M, Hagendoorn M, Mager WH, Planta RJ (1984) Structural comparison of yeast ribosomal protein genes. Nucleic Acids Res 12:6685–6700
Leer RJ, Van Raamsdonk-Duin M, Mager WH, Planta RJ (1985) Conserved sequences upstream of yeast ribosomal protein genes. Curr Genet 9:273–277
Mager WH, Planta RJ (1990) Multifunctional DNA-binding proteins mediate concerted transcription activation of yeast ribosomal protein genes. Biochim Biophys Acta 1050:351–355
Mager WH, Planta RJ (1991) Coordinate expression of ribosomal protein genes in yeast as a function of cellular growth rate. Mol Cell Biochem 104:181–187
Mbonyi K, Beullens M, Detremerie K, Geerts L, Thevelein J (1988) Requirement of one functional RAS gene and inability of an oncogenic ras variant to mediate the glucose-induced cyclic AMP signal in the yeast Saccharomyces cerevisiae. EMBO J 8:3051–3057
McMaster S, Carmichael G (1977) Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci USA 74:4835–4838
Müller G, Bandlow W (1991a). A CAMP-binding ectoprotein in the yeast Saccharomyces cerevisiae. Biochemistry 30:10181–10190
Müller G, Bandlow W (1991b) Two lipid-anchored cAMP-binding proteins in the yeast Saccharomyces cerevisiae are unrelated to the R subunit of cytoplasmic protein kinase A. Eur J Biochem 202:299–308
Planta RJ, Mager WH (1988) Coordinate control of ribosomal protein gene expression in yeast. In: Tuite MF, Picard M, Bolotin-Fukuhara M (eds) Genetics of Translation. Springer-Verlag, NATO ASU Series H, Vol 14, pp 117–129
Remacha M, Saenz-Robles M, Dolores Vilella M, Ballesta J (1988) Independent genes coding for three acidic proteins of the large ribosomal subunit from Saccharomyces cerevisiae. J Biol Chem 263:9094–9101
Rhode PR, Sweder KS, Oegema KF, Campbell JL (1989) The gene encoding ARS-binding factor I is essential for the viability of yeast. Genes Dev 3:1926–1939
Rhode PR, Elsasser S, Campbell H (1992) Role of multifunctional autonomously replicating sequence binding factor 1 in the initiation of DNA replication and transcriptional control in Saccharomyces cerevisiae. Mol Cell Biol 12:1064–1077
Rotenberg HO, Woolford JL (1986) Tripartite upstream promoter element essential for expression of Saccharomyces cerevisiae ribosomal protein genes. Mol Cell Biol 6:674–687
Santangelo G, Tornow J (1990) Efficient transcription of the glycolytic gene ADH1 and three translational component genes requires the GCR1 product, which can act through TUF/GRF/RAP binding sites. Mol Cell Biol 10:859–862
Seta FD, Ciafré S, Marck C, Santoro B, Presatti C, Sentenac A Bozzoni I (1990) The ABFI factor is the transcriptional activator of the L2 ribosomal protein genes in Saccharomyces cerevisiae. Mol Cell Biol 10:2437–2441
Shore D, Nasmyth K (1987) Purification and cloning of a DNA binding protein from yeast that binds to both silencer and activator elements. Cell 51:721–732
Sweder KS, Rhode PR, Campbell JL (1988) Purification and characterization of proteins that bind to yeast ARSs. J Biol Chem 263:17270–17277
Thevelein J (1991) Fermentable sugars and intracellular acidification as specific activators of the RAS-adenylate cyclase signalling pathway in yeast: the relationship to nutrient-induced cell cycle control. Mol Microbiol 5:1301–1307
Tortora P, Burline N, Caspani G, Guerritore A (1984) Studies on glucose-induced inactivation of gluconeogenetic enzymes in adenylate cyclase and cAMP-dependent protein kinase yeast mutants. Eur J Biochem 145:543–548
Tsang J, Henry Y, Chambers A, Kingsman A, Kingsman S (1990) Phosphorylation influences the binding of the yeast RAP1 protein to the upstream activating sequence of the PGK gene. Nucleic Acids Res 18:7331–7337
Van Aelst L, Boy-Marotte E, Camonis J, Thevelein J, Jacquer M, (1990) The C-terminal part of the CDC25 gene product plays a key role in signal transduction in the glucose-induced modulation of CAMP level in Saccharomyces cerevisiae. Eur J Biochem 193:675–680
Van Aelst L, Hohmann S, Zimmermann K, Jans A, Thevelein J (1991a) A yeast homologue of the bovine lens fiber MIP gene family complements the growth defect of a Saccharomyces cerevisiae mutant deficient in glucose-induced Ras-mediated cAMP signalling. EMBO J 10:2095–2104
Van Aelst L, Jans A, Thevelein J (1991b) Involvement of the CDC25 gene product in the signal transmission pathway of the glucose-induced RAS-mediated CAMP signal in the yeast Saccharomyces cerevisiae. J Gen. Microbiol 137:341–349
Woudt L, Smit A, Mager WH, Planta RJ (1986) Conserved sequence elements upstream of the gene encoding yeast ribosomal protein L25 are involved in transcription activation. EMBO J 5:1037–1040
Woudt LP, Mager WH, Nieuwint RTM, Wassenaar GM, Van der Kuyl AC, Murre JJ, Hoekman M, Brockhoff P, Planta RJ (1987) Analysis of upstream activation sites of yeast ribosomal protein genes. Nucleic Acids Res 15:6037–6048
Author information
Authors and Affiliations
Additional information
Communicated by C.P. Hollenberg
Rights and permissions
About this article
Cite this article
Kraakman, L.S., Griffioen, G., Zerp, S. et al. Growth-related expression of ribosomal protein genes in Saccharomyces cerevisiae . Molec. Gen. Genet. 239, 196–204 (1993). https://doi.org/10.1007/BF00281618
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00281618