Swi4-dependent SWI4 transcription couples cell size to cell cycle commitment

Growth-dependent accumulation of the G1/S transcription factor SBF, composed of Swi4 and Swi6, occurs in G1 phase in budding yeast and is limiting for commitment to division, termed Start. Here, we investigate the mechanisms for the size dependence of Swi4 accumulation using different genetic contex...

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Published iniScience Vol. 28; no. 3; p. 112027
Main Authors Goswami, Pooja, Ghimire, Abhishek, Coffin, Carleton, Cheng, Jing, Coulombe-Huntington, Jasmin, Ghazal, Ghada, Thattikota, Yogitha, Guerra, María Florencia, Tyers, Mike, Tollis, Sylvain, Royer, Catherine A.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 21.03.2025
Elsevier
Subjects
Cell biology
Molecular biology
Cell biology
Molecular biology
Online AccessGet full text
ISSN2589-0042
2589-0042
DOI10.1016/j.isci.2025.112027

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Abstract Growth-dependent accumulation of the G1/S transcription factor SBF, composed of Swi4 and Swi6, occurs in G1 phase in budding yeast and is limiting for commitment to division, termed Start. Here, we investigate the mechanisms for the size dependence of Swi4 accumulation using different genetic contexts and quantitative scanning number and brightness microscopy. Mutation of SBF binding sites in the SWI4 promoter or disruption of SBF activation resulted in ∼33–50% decrease in Swi4 accumulation rate and concordantly increased cell size at Start. Ectopic inducible expression of Swi4 in G1 phase cells increased production of Swi4 from the endogenous promoter, upregulated transcription of the G1/S regulon, and accelerated Start. A threshold model in which Swi4 titrates SBF binding sites in G1/S promoters predicted the effects of nutrients, ploidy, and G1/S regulatory mutations on cell size. These results exemplify how transcription factor auto-production can refine a cell state transition. [Display omitted] •Swi4 protein activates SWI4 transcription in a Swi4 binding site dependent manner•Ectopic expression of Swi4 induces SWI4 expression and accelerates the G1/S transition•Quantitative microscopy suggests a copy-number threshold Swi4 is required for Start•A Swi4 threshold predicts cell size in different genetic and nutritional contexts Molecular biology; Cell biology
AbstractList Growth-dependent accumulation of the G1/S transcription factor SBF, composed of Swi4 and Swi6, occurs in G1 phase in budding yeast and is limiting for commitment to division, termed Start. Here, we investigate the mechanisms for the size dependence of Swi4 accumulation using different genetic contexts and quantitative scanning number and brightness microscopy. Mutation of SBF binding sites in the SWI4 promoter or disruption of SBF activation resulted in ∼33-50% decrease in Swi4 accumulation rate and concordantly increased cell size at Start. Ectopic inducible expression of Swi4 in G1 phase cells increased production of Swi4 from the endogenous promoter, upregulated transcription of the G1/S regulon, and accelerated Start. A threshold model in which Swi4 titrates SBF binding sites in G1/S promoters predicted the effects of nutrients, ploidy, and G1/S regulatory mutations on cell size. These results exemplify how transcription factor auto-production can refine a cell state transition.Growth-dependent accumulation of the G1/S transcription factor SBF, composed of Swi4 and Swi6, occurs in G1 phase in budding yeast and is limiting for commitment to division, termed Start. Here, we investigate the mechanisms for the size dependence of Swi4 accumulation using different genetic contexts and quantitative scanning number and brightness microscopy. Mutation of SBF binding sites in the SWI4 promoter or disruption of SBF activation resulted in ∼33-50% decrease in Swi4 accumulation rate and concordantly increased cell size at Start. Ectopic inducible expression of Swi4 in G1 phase cells increased production of Swi4 from the endogenous promoter, upregulated transcription of the G1/S regulon, and accelerated Start. A threshold model in which Swi4 titrates SBF binding sites in G1/S promoters predicted the effects of nutrients, ploidy, and G1/S regulatory mutations on cell size. These results exemplify how transcription factor auto-production can refine a cell state transition.
Growth-dependent accumulation of the G1/S transcription factor SBF, composed of Swi4 and Swi6, occurs in G1 phase in budding yeast and is limiting for commitment to division, termed Start. Here, we investigate the mechanisms for the size dependence of Swi4 accumulation using different genetic contexts and quantitative scanning number and brightness microscopy. Mutation of SBF binding sites in the promoter or disruption of SBF activation resulted in ∼33-50% decrease in Swi4 accumulation rate and concordantly increased cell size at Start. Ectopic inducible expression of Swi4 in G1 phase cells increased production of Swi4 from the endogenous promoter, upregulated transcription of the G1/S regulon, and accelerated Start. A threshold model in which Swi4 titrates SBF binding sites in G1/S promoters predicted the effects of nutrients, ploidy, and G1/S regulatory mutations on cell size. These results exemplify how transcription factor auto-production can refine a cell state transition.
Growth-dependent accumulation of the G1/S transcription factor SBF, composed of Swi4 and Swi6, occurs in G1 phase in budding yeast and is limiting for commitment to division, termed Start. Here, we investigate the mechanisms for the size dependence of Swi4 accumulation using different genetic contexts and quantitative scanning number and brightness microscopy. Mutation of SBF binding sites in the SWI4 promoter or disruption of SBF activation resulted in ∼33–50% decrease in Swi4 accumulation rate and concordantly increased cell size at Start. Ectopic inducible expression of Swi4 in G1 phase cells increased production of Swi4 from the endogenous promoter, upregulated transcription of the G1/S regulon, and accelerated Start. A threshold model in which Swi4 titrates SBF binding sites in G1/S promoters predicted the effects of nutrients, ploidy, and G1/S regulatory mutations on cell size. These results exemplify how transcription factor auto-production can refine a cell state transition. • Swi4 protein activates SWI4 transcription in a Swi4 binding site dependent manner • Ectopic expression of Swi4 induces SWI4 expression and accelerates the G1/S transition • Quantitative microscopy suggests a copy-number threshold Swi4 is required for Start • A Swi4 threshold predicts cell size in different genetic and nutritional contexts Molecular biology; Cell biology
Growth-dependent accumulation of the G1/S transcription factor SBF, composed of Swi4 and Swi6, occurs in G1 phase in budding yeast and is limiting for commitment to division, termed Start. Here, we investigate the mechanisms for the size dependence of Swi4 accumulation using different genetic contexts and quantitative scanning number and brightness microscopy. Mutation of SBF binding sites in the SWI4 promoter or disruption of SBF activation resulted in ∼33–50% decrease in Swi4 accumulation rate and concordantly increased cell size at Start. Ectopic inducible expression of Swi4 in G1 phase cells increased production of Swi4 from the endogenous promoter, upregulated transcription of the G1/S regulon, and accelerated Start. A threshold model in which Swi4 titrates SBF binding sites in G1/S promoters predicted the effects of nutrients, ploidy, and G1/S regulatory mutations on cell size. These results exemplify how transcription factor auto-production can refine a cell state transition. [Display omitted] •Swi4 protein activates SWI4 transcription in a Swi4 binding site dependent manner•Ectopic expression of Swi4 induces SWI4 expression and accelerates the G1/S transition•Quantitative microscopy suggests a copy-number threshold Swi4 is required for Start•A Swi4 threshold predicts cell size in different genetic and nutritional contexts Molecular biology; Cell biology
Growth-dependent accumulation of the G1/S transcription factor SBF, composed of Swi4 and Swi6, occurs in G1 phase in budding yeast and is limiting for commitment to division, termed Start. Here, we investigate the mechanisms for the size dependence of Swi4 accumulation using different genetic contexts and quantitative scanning number and brightness microscopy. Mutation of SBF binding sites in the SWI4 promoter or disruption of SBF activation resulted in ∼33–50% decrease in Swi4 accumulation rate and concordantly increased cell size at Start. Ectopic inducible expression of Swi4 in G1 phase cells increased production of Swi4 from the endogenous promoter, upregulated transcription of the G1/S regulon, and accelerated Start. A threshold model in which Swi4 titrates SBF binding sites in G1/S promoters predicted the effects of nutrients, ploidy, and G1/S regulatory mutations on cell size. These results exemplify how transcription factor auto-production can refine a cell state transition.
ArticleNumber 112027
Author Guerra, María Florencia
Tollis, Sylvain
Goswami, Pooja
Ghimire, Abhishek
Ghazal, Ghada
Royer, Catherine A.
Cheng, Jing
Thattikota, Yogitha
Tyers, Mike
Coffin, Carleton
Coulombe-Huntington, Jasmin
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Present address: Department of Neurology, Brain Science Institute, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
Present address: Department of Bioengineering, McGill University, Montreal, QC H3A 0E9, Canada
Present address: Institute of Biomedicine, School of Medicine, Faculty of Health Sciences, University of Eastern Finland, Joensuu, 70211 Kuopio, Finland
Present address: Montreal Neurological Institute, McGill University, Montréal, QC H3A 2B4, Canada
These authors contributed equally
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Snippet Growth-dependent accumulation of the G1/S transcription factor SBF, composed of Swi4 and Swi6, occurs in G1 phase in budding yeast and is limiting for...
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SubjectTerms Cell biology
Molecular biology
Title Swi4-dependent SWI4 transcription couples cell size to cell cycle commitment
URI https://dx.doi.org/10.1016/j.isci.2025.112027
https://www.ncbi.nlm.nih.gov/pubmed/40124484
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