This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by French, S. L.
Right arrow Articles by Beyer, A. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by French, S. L.
Right arrow Articles by Beyer, A. L.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, March 2003, p. 1558-1568, Vol. 23, No. 5
0270-7306/03/$08.00+0     DOI: 10.1128/MCB.23.5.1558-1568.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

In Exponentially Growing Saccharomyces cerevisiae Cells, rRNA Synthesis Is Determined by the Summed RNA Polymerase I Loading Rate Rather than by the Number of Active Genes

Sarah L. French,1 Yvonne N. Osheim,1 Francesco Cioci,2 Masayasu Nomura,2 and Ann L. Beyer1*

Department of Microbiology, University of Virginia Health System, Charlottesville, Virginia 22908-0734,1 Department of Biological Chemistry, University of California, Irvine, California 92717-17002

Received 26 August 2002/ Returned for modification 3 October 2002/ Accepted 13 December 2002

Genes encoding rRNA are multicopy and thus could be regulated by changing the number of active genes or by changing the transcription rate per gene. We tested the hypothesis that the number of open genes is limiting rRNA synthesis by using an electron microscopy method that allows direct counting of the number of active genes per nucleolus and the number of polymerases per active gene. Two strains of Saccharomyces cerevisiae were analyzed during exponential growth: a control strain with a typical number of rRNA genes (~143 in this case) and a strain in which the rRNA gene number was reduced to ~42 but which grows as well as controls. In control strains, somewhat more than half of the genes were active and the mean number of polymerases/gene was ~50 ± 20. In the 42-copy strain, all rRNA genes were active with a mean number of 100 ± 29 polymerases/gene. Thus, an equivalent number of polymerases was active per nucleolus in the two strains, though the number of active genes varied by twofold, showing that overall initiation rate, and not the number of active genes, determines rRNA transcription rate during exponential growth in yeast. Results also allow an estimate of elongation rate of ~60 nucleotides/s for yeast Pol I and a reinitiation rate of less than 1 s on the most heavily transcribed genes.


* Corresponding author. Mailing address: Department of Microbiology, Box 800734, University of Virginia Health System, Charlottesville, VA 22908-0734. Phone: (434) 924-5611. Fax: (434) 982-1071. E-mail: alb4h{at}virginia.edu.


Molecular and Cellular Biology, March 2003, p. 1558-1568, Vol. 23, No. 5
0022-538X/03/$08.00+0     DOI: 10.1128/MCB.23.5.1558-1568.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.




This article has been cited by other articles:

  • Hontz, R. D., Niederer, R. O., Johnson, J. M., Smith, J. S. (2009). Genetic Identification of Factors That Modulate Ribosomal DNA Transcription in Saccharomyces cerevisiae. Genetics 182: 105-119 [Abstract] [Full Text]  
  • James, S. A., O'Kelly, M. J.T., Carter, D. M., Davey, R. P., van Oudenaarden, A., Roberts, I. N. (2009). Repetitive sequence variation and dynamics in the ribosomal DNA array of Saccharomyces cerevisiae as revealed by whole-genome resequencing. Genome Res 19: 626-635 [Abstract] [Full Text]  
  • Paredes, S., Maggert, K. A. (2009). Expression of I-CreI Endonuclease Generates Deletions Within the rDNA of Drosophila. Genetics 181: 1661-1671 [Abstract] [Full Text]  
  • Zhang, Y., Sikes, M. L., Beyer, A. L., Schneider, D. A. (2009). The Paf1 complex is required for efficient transcription elongation by RNA polymerase I. Proc. Natl. Acad. Sci. USA 106: 2153-2158 [Abstract] [Full Text]  
  • Dimelow, R. J, Wilkinson, S. J (2009). Control of translation initiation: a model-based analysis from limited experimental data. J R Soc Interface 6: 51-61 [Abstract] [Full Text]  
  • Sanij, E., Poortinga, G., Sharkey, K., Hung, S., Holloway, T. P., Quin, J., Robb, E., Wong, L. H., Thomas, W. G., Stefanovsky, V., Moss, T., Rothblum, L., Hannan, K. M., McArthur, G. A., Pearson, R. B., Hannan, R. D. (2008). UBF levels determine the number of active ribosomal RNA genes in mammals. JCB 183: 1259-1274 [Abstract] [Full Text]  
  • Hontz, R. D., French, S. L., Oakes, M. L., Tongaonkar, P., Nomura, M., Beyer, A. L., Smith, J. S. (2008). Transcription of Multiple Yeast Ribosomal DNA Genes Requires Targeting of UAF to the Promoter by Uaf30. Mol. Cell. Biol. 28: 6709-6719 [Abstract] [Full Text]  
  • French, S. L., Osheim, Y. N., Schneider, D. A., Sikes, M. L., Fernandez, C. F., Copela, L. A., Misra, V. A., Nomura, M., Wolin, S. L., Beyer, A. L. (2008). Visual Analysis of the Yeast 5S rRNA Gene Transcriptome: Regulation and Role of La Protein. Mol. Cell. Biol. 28: 4576-4587 [Abstract] [Full Text]  
  • Merz, K., Hondele, M., Goetze, H., Gmelch, K., Stoeckl, U., Griesenbeck, J. (2008). Actively transcribed rRNA genes in S. cerevisiae are organized in a specialized chromatin associated with the high-mobility group protein Hmo1 and are largely devoid of histone molecules. Genes Dev. 22: 1190-1204 [Abstract] [Full Text]  
  • Kawauchi, J., Mischo, H., Braglia, P., Rondon, A., Proudfoot, N. J. (2008). Budding yeast RNA polymerases I and II employ parallel mechanisms of transcriptional termination. Genes Dev. 22: 1082-1092 [Abstract] [Full Text]  
  • Haanstra, J. R., Stewart, M., Luu, V.-D., van Tuijl, A., Westerhoff, H. V., Clayton, C., Bakker, B. M. (2008). Control and Regulation of Gene Expression: QUANTITATIVE ANALYSIS OF THE EXPRESSION OF PHOSPHOGLYCERATE KINASE IN BLOODSTREAM FORM TRYPANOSOMA BRUCEI. J. Biol. Chem. 283: 2495-2507 [Abstract] [Full Text]  
  • Catala, M., Tremblay, M., Samson, E., Conconi, A., Abou Elela, S. (2008). Deletion of Rnt1p Alters the Proportion of Open versus Closed rRNA Gene Repeats in Yeast. Mol. Cell. Biol. 28: 619-629 [Abstract] [Full Text]  
  • Johzuka, K., Horiuchi, T. (2007). RNA polymerase I transcription obstructs condensin association with 35S rRNA coding regions and can cause contraction of long repeat in Saccharomyces cerevisiae. GENES CELLS 12: 759-771 [Abstract] [Full Text]  
  • Dasgupta, A., Sprouse, R. O., French, S., Aprikian, P., Hontz, R., Juedes, S. A., Smith, J. S., Beyer, A. L., Auble, D. T. (2007). Regulation of rRNA Synthesis by TATA-Binding Protein-Associated Factor Mot1. Mol. Cell. Biol. 27: 2886-2896 [Abstract] [Full Text]  
  • Pontvianne, F., Matia, I., Douet, J., Tourmente, S., Medina, F. J., Echeverria, M., Saez-Vasquez, J. (2007). Characterization of AtNUC-L1 Reveals a Central Role of Nucleolin in Nucleolus Organization and Silencing of AtNUC-L2 Gene in Arabidopsis. Mol. Biol. Cell 18: 369-379 [Abstract] [Full Text]  
  • Grenetier, S., Bouchoux, C., Goguel, V. (2006). CTD kinase I is required for the integrity of the rDNA tandem array. Nucleic Acids Res 34: 4996-5006 [Abstract] [Full Text]  
  • Schneider, D. A., French, S. L., Osheim, Y. N., Bailey, A. O., Vu, L., Dodd, J., Yates, J. R., Beyer, A. L., Nomura, M. (2006). RNA polymerase II elongation factors Spt4p and Spt5p play roles in transcription elongation by RNA polymerase I and rRNA processing. Proc. Natl. Acad. Sci. USA 103: 12707-12712 [Abstract] [Full Text]  
  • Oakes, M. L., Johzuka, K., Vu, L., Eliason, K., Nomura, M. (2006). Expression of rRNA Genes and Nucleolus Formation at Ectopic Chromosomal Sites in the Yeast Saccharomyces cerevisiae.. Mol. Cell. Biol. 26: 6223-6238 [Abstract] [Full Text]  
  • Kim, Y.-H., Ishikawa, D., Ha, H. P., Sugiyama, M., Kaneko, Y., Harashima, S. (2006). Chromosome XII context is important for rDNA function in yeast. Nucleic Acids Res 34: 2914-2924 [Abstract] [Full Text]  
  • Oakes, M. L., Siddiqi, I., French, S. L., Vu, L., Sato, M., Aris, J. P., Beyer, A. L., Nomura, M. (2006). Role of Histone Deacetylase Rpd3 in Regulating rRNA Gene Transcription and Nucleolar Structure in Yeast. Mol. Cell. Biol. 26: 3889-3901 [Abstract] [Full Text]  
  • Earley, K., Lawrence, R. J., Pontes, O., Reuther, R., Enciso, A. J., Silva, M., Neves, N., Gross, M., Viegas, W., Pikaard, C. S. (2006). Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev. 20: 1283-1293 [Abstract] [Full Text]  
  • Johzuka, K., Terasawa, M., Ogawa, H., Ogawa, T., Horiuchi, T. (2006). Condensin Loaded onto the Replication Fork Barrier Site in the rRNA Gene Repeats during S Phase in a FOB1-Dependent Fashion To Prevent Contraction of a Long Repetitive Array in Saccharomyces cerevisiae.. Mol. Cell. Biol. 26: 2226-2236 [Abstract] [Full Text]  
  • Meraner, J., Lechner, M., Loidl, A., Goralik-Schramel, M., Voit, R., Grummt, I., Loidl, P. (2006). Acetylation of UBF changes during the cell cycle and regulates the interaction of UBF with RNA polymerase I.. Nucleic Acids Res 34: 1798-1806 [Abstract] [Full Text]  
  • Caburet, S., Conti, C., Schurra, C., Lebofsky, R., Edelstein, S. J., Bensimon, A. (2005). Human ribosomal RNA gene arrays display a broad range of palindromic structures. Genome Res 15: 1079-1085 [Abstract] [Full Text]  
  • Tongaonkar, P., French, S. L., Oakes, M. L., Vu, L., Schneider, D. A., Beyer, A. L., Nomura, M. (2005). Histones are required for transcription of yeast rRNA genes by RNA polymerase I. Proc. Natl. Acad. Sci. USA 102: 10129-10134 [Abstract] [Full Text]  
  • Hoang, T., Peng, W.-T., Vanrobays, E., Krogan, N., Hiley, S., Beyer, A. L., Osheim, Y. N., Greenblatt, J., Hughes, T. R., Lafontaine, D. L. J. (2005). Esf2p, a U3-Associated Factor Required for Small-Subunit Processome Assembly and Compaction. Mol. Cell. Biol. 25: 5523-5534 [Abstract] [Full Text]  
  • Michel, A. H., Kornmann, B., Dubrana, K., Shore, D. (2005). Spontaneous rDNA copy number variation modulates Sir2 levels and epigenetic gene silencing. Genes Dev. 19: 1199-1210 [Abstract] [Full Text]  
  • Meier, A., Thoma, F. (2005). RNA Polymerase I Transcription Factors in Active Yeast rRNA Gene Promoters Enhance UV Damage Formation and Inhibit Repair. Mol. Cell. Biol. 25: 1586-1595 [Abstract] [Full Text]  
  • Prescott, E. M., Osheim, Y. N., Jones, H. S., Alen, C. M., Roan, J. G., Reeder, R. H., Beyer, A. L., Proudfoot, N. J. (2004). Transcriptional termination by RNA polymerase I requires the small subunit Rpa12p. Proc. Natl. Acad. Sci. USA 101: 6068-6073 [Abstract] [Full Text]  
  • Probst, A. V., Fagard, M., Proux, F., Mourrain, P., Boutet, S., Earley, K., Lawrence, R. J., Pikaard, C. S., Murfett, J., Furner, I., Vaucheret, H., Scheid, O. M. (2004). Arabidopsis Histone Deacetylase HDA6 Is Required for Maintenance of Transcriptional Gene Silencing and Determines Nuclear Organization of rDNA Repeats. Plant Cell 16: 1021-1034 [Abstract] [Full Text]  
  • Claypool, J. A., French, S. L., Johzuka, K., Eliason, K., Vu, L., Dodd, J. A., Beyer, A. L., Nomura, M. (2004). Tor Pathway Regulates Rrn3p-dependent Recruitment of Yeast RNA Polymerase I to the Promoter but Does Not Participate in Alteration of the Number of Active Genes. Mol. Biol. Cell 15: 946-956 [Abstract] [Full Text]  
  • Kobayashi, T. (2003). The Replication Fork Barrier Site Forms a Unique Structure with Fob1p and Inhibits the Replication Fork. Mol. Cell. Biol. 23: 9178-9188 [Abstract] [Full Text]  
  • Pontes, O., Lawrence, R. J., Neves, N., Silva, M., Lee, J.-H., Chen, Z. J., Viegas, W., Pikaard, C. S. (2003). Natural variation in nucleolar dominance reveals the relationship between nucleolus organizer chromatin topology and rRNA gene transcription in Arabidopsis. Proc. Natl. Acad. Sci. USA 100: 11418-11423 [Abstract] [Full Text]  
  • Grummt, I. (2003). Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev. 17: 1691-1702 [Full Text]  
  • Takeuchi, Y., Horiuchi, T., Kobayashi, T. (2003). Transcription-dependent recombination and the role of fork collision in yeast rDNA. Genes Dev. 17: 1497-1506 [Abstract] [Full Text]