SFP1 is involved in cell size modulation in respiro‐fermentative growth conditions

Saccharomyces cerevisiae grows fast on glucose, while growth slows down on ethanol as cells move from glucose fermentation to oxidative metabolism. The type of carbon source influences both the specific growth rate and cell cycle progression, as well as cell size. Yeast cells grown on glucose have a larger size than cells grown on ethanol. Here, we analysed the behaviour of a sfp1 null mutant during balanced and transitory states of growth in batch in response to changes in the growth medium carbon sources. In a screening for mutants affected in cell size at Start, SFP1 has been identified as a gene whose deletion caused one of the smallest whi phenotype. Findings presented in this work indicate that in the sfp1 null mutant the reduction in cell size is not only a consequence of the reduced growth rate but it is tightly linked to the cellular metabolism. The SFP1 gene product is required to sustain the increase of both rRNA and protein content that in wild‐type cells takes place in respiro‐fermentative growth conditions, while it seems dispensable for growth on non‐fermentable carbon sources. It follows that sfp1 cells growing on ethanol have a larger size than cells growing on glucose and, noticeably, the former enter the S phase with a critical cell size higher than the latter. These features, combined with the role of Sfp1p as a transcriptional factor, suggest that Sfp1p could be an important element in the control of the cell size modulated by nutrients. Copyright © 2005 John Wiley & Sons, Ltd.

[1]  B. Futcher,et al.  Cyclins and the Wiring of the Yeast Cell Cycle , 1996, Yeast.

[2]  Ronald W. Davis,et al.  Systematic screen for human disease genes in yeast , 2002, Nature Genetics.

[3]  E S Lander,et al.  Ploidy regulation of gene expression. , 1999, Science.

[4]  J. Broach,et al.  Efficient transition to growth on fermentable carbon sources in Saccharomyces cerevisiae requires signaling through the Ras pathway , 1998, The EMBO journal.

[5]  I. Rupeš,et al.  Checking cell size in yeast. , 2002, Trends in genetics : TIG.

[6]  Laura L. Newcomb,et al.  Glucose Regulation of Saccharomyces cerevisiae Cell Cycle Genes , 2003, Eukaryotic Cell.

[7]  T. P. Neufeld,et al.  Connections between growth and the cell cycle. , 1998, Current opinion in cell biology.

[8]  L. Alberghina,et al.  Structural heterogeneity in populations of the budding yeast Saccharomyces cerevisiae , 1983, Journal of bacteriology.

[9]  J. Pronk,et al.  The Saccharomyces cerevisiae acetyl-coenzyme A synthetase encoded by the ACS1 gene, but not the ACS2-encoded enzyme, is subject to glucose catabolite inactivation. , 1997, FEMS microbiology letters.

[10]  M. Mendenhall,et al.  Regulation of Cdc28 Cyclin-Dependent Protein Kinase Activity during the Cell Cycle of the Yeast Saccharomyces cerevisiae , 1998, Microbiology and Molecular Biology Reviews.

[11]  L. Alberghina,et al.  Quantitative flow cytometry: analysis of protein distributions in budding yeast. A mini-review. , 1993, Yeast.

[12]  C. Wittenberg,et al.  Regulation of Cell Size by Glucose Is Exerted via Repression of the CLN1 Promoter , 1998, Molecular and Cellular Biology.

[13]  M. Polymenis,et al.  Coordination of cell growth with cell division. , 1999, Current opinion in genetics & development.

[14]  D. Kressler,et al.  Synthetic Lethality with Conditional dbp6 Alleles Identifies Rsa1p, a Nucleoplasmic Protein Involved in the Assembly of 60S Ribosomal Subunits , 1999, Molecular and Cellular Biology.

[15]  C. Woldringh,et al.  Volume growth of daughter and parent cells during the cell cycle of Saccharomyces cerevisiae a/alpha as determined by image cytometry , 1993, Journal of bacteriology.

[16]  M. Tyers,et al.  A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. , 2004, Genes & development.

[17]  P. Lord,et al.  Variability in individual cell cycles of Saccharomyces cerevisiae. , 1981, Journal of cell science.

[18]  Saeed Tavazoie,et al.  Ras and Gpa2 Mediate One Branch of a Redundant Glucose Signaling Pathway in Yeast , 2004, PLoS biology.

[19]  L. Alberghina,et al.  Glucose metabolism and cell size in continuous cultures of Saccharomyces cerevisiae. , 2003, FEMS microbiology letters.

[20]  Filip Rolland,et al.  Glucose-sensing and -signalling mechanisms in yeast. , 2002, FEMS yeast research.

[21]  Mike Tyers,et al.  Systematic Identification of Pathways That Couple Cell Growth and Division in Yeast , 2002, Science.

[22]  K Nasmyth,et al.  CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. , 1993, Genes & development.

[23]  Mark Johnston,et al.  Grr1 of Saccharomyces cerevisiae is connected to the ubiquitin proteolysis machinery through Skp1: coupling glucose sensing to gene expression and the cell cycle , 1997, The EMBO journal.

[24]  D. Koller,et al.  Sfp1 is a stress- and nutrient-sensitive regulator of ribosomal protein gene expression. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[25]  L. Johnston,et al.  Getting started: regulating the initiation of DNA replication in yeast. , 1997, Annual review of microbiology.

[26]  L. Hartwell,et al.  Unequal division in Saccharomyces cerevisiae and its implications for the control of cell division , 1977, The Journal of cell biology.

[27]  B. Carter,et al.  The relationship between cell size and cell division in the yeast Saccharomyces cerevisiae. , 1978, Experimental cell research.

[28]  B. Carter,et al.  Genetic control of cell division in yeast cultured at different growth rates , 1977, Nature.

[29]  K. Nasmyth,et al.  Yeast G1 cyclins CLN1 and CLN2 and a GAP‐like protein have a role in bud formation. , 1993, The EMBO journal.

[30]  L. Alberghina,et al.  Control of the yeast cell cycle by protein synthesis. , 1982, Experimental cell research.

[31]  Ian M. Fingerman,et al.  Sfp1 Plays a Key Role in Yeast Ribosome Biogenesis , 2003, Eukaryotic Cell.

[32]  H. Y. Steensma,et al.  Regulation of alcoholic fermentation in batch and chemostat cultures of Kluyveromyces lactis CBS 2359 , 1998, Yeast.

[33]  L. Alberghina,et al.  A double flow cytometric tag allows tracking of the dynamics of cell cycle progression of newborn Saccharomyces cerevisiae cells during balanced exponential growth , 1995, Yeast.

[34]  L. Alberghina,et al.  Flow Cytometry and Cell Cycle Kinetics in Continuous and Fed‐Batch Fermentations of Budding Yeast , 1991, Biotechnology progress.

[35]  L. Hartwell.  Saccharomyces cerevisiae cell cycle. , 1974, Bacteriological reviews.

[36]  Lilia Alberghina,et al.  Control by Nutrients of Growth and Cell Cycle Progression in Budding Yeast, Analyzed by Double-Tag Flow Cytometry , 1998, Journal of bacteriology.

[37]  J. D. de Winde,et al.  Novel sensing mechanisms and targets for the cAMP–protein kinase A pathway in the yeast Saccharomyces cerevisiae , 1999, Molecular microbiology.

[38]  L. Hartwell,et al.  Asymmetrical division of Saccharomyces cerevisiae , 1980, Journal of bacteriology.

[39]  E. O’Shea,et al.  Pho85 and signaling environmental conditions. , 2002, Trends in biochemical sciences.

[40]  G. C. Johnston,et al.  RNA synthesis and control of cell division in the yeast S. cerevisiae , 1978, Cell.

[41]  P. Lord,et al.  Dependency of size of Saccharomyces cerevisiae cells on growth rate , 1979, Journal of bacteriology.

[42]  J. Winderickx,et al.  From feast to famine; adaptation to nutrient availability in yeast , 2003 .