Septins localize to microtubules during nutritional limitation in Saccharomyces cerevisiae

Abstract

BackgroundIn Saccharomyces cerevisiae, nutrient limitation stimulates diploid cells to undergo DNA replication and meiosis, followed by the formation of four haploid spores. Septins are a family of proteins that assemble a ring structure at the mother-daughter neck during vegetative growth, where they control cytokinesis. In sporulating cells, the septin ring disassembles and septins relocalize to the prospore membrane.ResultsHere, we demonstrate that nutrient limitation triggers a change in the localization of at least two vegetative septins (Cdc10 and Cdc11) from the bud neck to the microtubules. The association of Cdc10 and Cdc11 with microtubules persists into meiosis, and they are found associated with the meiotic spindle until the end of meiosis II. In addition, the meiosis-specific septin Spr28 displays similar behavior, suggesting that this is a common feature of septins. Septin association to microtubules is a consequence of the nutrient limitation signal, since it is also observed when haploid cells are incubated in sporulation medium and when haploid or diploid cells are grown in medium containing non-fermentable carbon sources. Moreover, during meiosis II, when the nascent prospore membrane is formed, septins moved from the microtubules to this membrane. Proper organization of the septins on the membrane requires the sporulation-specific septins Spr3 and Spr28.ConclusionNutrient limitation in S. cerevisiae triggers the sporulation process, but it also induces the disassembly of the septin bud neck ring and relocalization of the septin subunits to the nucleus. Septins remain associated with microtubules during the meiotic divisions and later, during spore morphogenesis, they are detected associated to the nascent prospore membranes surrounding each nuclear lobe. Septin association to microtubules also occurs during growth in non-fermentable carbon sources.

Sporulation in the Budding Yeast Saccharomyces cerevisiae

“…The higher order organization of the septin filaments on the prospore membrane is not known. When ectopically expressed in vegetative cells, Spr3 is not incorporated into septin filaments at the bud neck; reciprocally, Cdc12 is present during sporulation but does not enter the septin structures on the prospore membrane (Fares et al 1996;McMurray and Thorner 2008;Pablo-Hernando et al 2008). These observations, along with the dynamic rather than static behavior of the septins, suggest that the organization of septins at the prospore membrane is different from that at the bud neck.…”

“…Loss of Spr28, which is predicted to sit at the ends of the octamer, disrupts the bar-like organization and the remaining septins distribute uniformly around the prospore membrane as it expands (PabloHernando et al 2008). Deleting SPR3 causes loss of the bar structure plus greatly reduced association of the remaining septins with the prospore membrane (Fares et al 1996;Pablo-Hernando et al 2008). The higher order organization of the septin filaments on the prospore membrane is not known.…”

The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species

“…Septin filaments are organized by two tetramers that linearly assemble Cdc3p, Cdc10p, Cdc11p, and Cdc12p in vegetative cells (1204). Two sporulation-specific septins, Spr3p and Spr28p, replace Cdc11p and Cdc12p to compose the tetramers during the formation of the prospore membrane (1205). A Gip1p-Glc7p phosphatase complex is required for the proper localization of septin bars to the prospore membrane (1206).…”

Off-Target Effects of the Septin Drug Forchlorfenuron on Nonplant Eukaryotes

“…For example, in cdc10⌬ and shs1⌬ cells, certain glucose-repressed genes are inappropriately derepressed (58) and a septin-dependent diffusion barrier at the midzone of zygotes regulates the timing of mixing of parental mitochondria (59), but these findings do not readily explain our observations. Notably, nutrient limitation, which could mimic mitochondrial dysfunction, drives colocalization of budding yeast septins with microtubules in long, fiber-like structures reminiscent of those induced by FCF (60). However, we determined, using a GFP-tagged tubulin construct, that FCF-induced septin fibers do not colocalize with microtubules (L. R. Heasley and M. A. McMurray, unpublished data).…”