Cell cycle control of septin ring dynamics in the budding yeast.
Septins constitute a cytoskeletal structure that is conserved in eukaryotes. In Saccharomyces cerevisiae, the Cdc3, Cdc10, Cdc11, Cdc12 and Shs1/Sep7 septins assemble as a ring that marks the cytokinetic plane throughout the budding cycle. This structure participates in different aspects of morphogenesis, such as selection of cell polarity, localization of chitin synthesis, the switch from hyperpolar to isotropic bud growth after bud emergence and the spatial regulation of septation. The septin cytoskeleton assembles at the pre-bud site before bud emergence, remains there during bud growth and duplicates at late mitosis eventually disappearing after cell separation. Using a septin-GFP fusion and time-lapse confocal microscopy, we have determined that septin dynamics are maintained in budding zygotes and during unipolar synchronous growth in pseudohyphae. By means of specific cell cycle arrests and deregulation of cell cycle controls we show that septin assembly is dependent on G1 cyclin/Cdc28-mediated cell cycle signals and that the small GTPase Cdc42, but not Rho1, are essential for this event. However, during bud growth, the septin ring shapes a bud-neck-spanning structure that is unaffected by failures in the regulation of mitosis, such as activation of the DNA repair or spindle assembly checkpoints or inactivation of the anaphase-promoting complex (APC). At the end of the cell cycle, the splitting of the ring into two independent structures depends on the function of the mitotic exit network in which the protein phosphatase Cdc14 participates. Our data support a role of cell cycle control mechanisms in the regulation of septin dynamics to accurately coordinate morphogenesis throughout the budding process in yeast.
Cid
Vı Ctor J
VCJ
Departamento de Microbiologı́a II, Facultad de Farmacia, Universidad Complutense, 28040-Madrid, Spain1.
Adamiková
Lubica
L
Department of Biochemistry, Comenius University, Faculty of Natural Sciences, Mlynská dolina CH-1, 842 15 Bratislava, Slovakia2.
Sánchez
Miguel
M
Departamento de Biologı́a y Genética. Edificio Departamental, Campus Miguel de Unamuno, Universidad de Salamanca, 37007, Salamanca, Spain3.
Molina
Marı A
MA
Departamento de Microbiologı́a II, Facultad de Farmacia, Universidad Complutense, 28040-Madrid, Spain1.
Nombela
César
C
Departamento de Microbiologı́a II, Facultad de Farmacia, Universidad Complutense, 28040-Madrid, Spain1.
D064173:Anaphase-Promoting Complex-Cyclosome; D018797:Cell Cycle Proteins / Q000235:genetics / Q000378:metabolism*; D003598:Cytoskeletal Proteins / Q000235:genetics / Q000378:metabolism*; D020558:GTP Phosphohydrolases; D015966:Gene Expression Regulation, Fungal; D049452:Green Fluorescent Proteins; D008025:Ligases / Q000235:genetics / Q000378:metabolism; D008164:Luminescent Proteins / Q000235:genetics / Q000378:metabolism; D008565:Membrane Proteins; D018613:Microscopy, Confocal; D008938:Mitosis; D011993:Recombinant Fusion Proteins / Q000235:genetics / Q000378:metabolism; D012441:Saccharomyces cerevisiae / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D029701:Saccharomyces cerevisiae Proteins; D029702:Schizosaccharomyces pombe Proteins; D015398:Signal Transduction; D014157:Transcription Factors; D043743:Ubiquitin-Protein Ligase Complexes; D044767:Ubiquitin-Protein Ligases; D020846:cdc42 GTP-Binding Protein, Saccharomyces cerevisiae / Q000235:genetics / Q000378:metabolism; D020741:rho GTP-Binding Proteins / Q000235:genetics / Q000378:metabolism
D018797:Cell Cycle Proteins; D003598:Cytoskeletal Proteins; D008164:Luminescent Proteins; D008565:Membrane Proteins; D011993:Recombinant Fusion Proteins; D029701:Saccharomyces cerevisiae Proteins; D029702:Schizosaccharomyces pombe Proteins; D014157:Transcription Factors; C061178:cdc10 protein, S pombe; D049452:Green Fluorescent Proteins; D043743:Ubiquitin-Protein Ligase Complexes; D064173:Anaphase-Promoting Complex-Cyclosome; D044767:Ubiquitin-Protein Ligases; C512892:CDC10 protein, S cerevisiae; D020558:GTP Phosphohydrolases; C051302:RHO1 protein, S cerevisiae; D020846:cdc42 GTP-Binding Protein, Saccharomyces cerevisiae; D020741:rho GTP-Binding Proteins; D008025:Ligases