Sporulation in the Budding Yeast <i>Saccharomyces cerevisiae</i>

Neiman, Aaron M.

doi:10.1534/genetics.111.127126

Cited by 350 publications

(415 citation statements)

References 293 publications

(445 reference statements)

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“…Sporulation in S. cerevisiae occurs as diploid cells experience nutritional stress. The diploid mother cell undergoes meiosis and spore formation, creating four haploid spores, the yeast equivalent of gametes (Neiman 2011 nuclei formed during meiosis are encapsulated in a double lipid bilayer membrane called the prospore membrane (PSM). The PSM forms de novo after meiosis II (Neiman 1998) and ultimately surrounds each of the haploid nuclei.…”

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Timely Closure of the Prospore Membrane Requires SPS1 and SPO77 in Saccharomyces cerevisiae

et al. 2016

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During sporulation in Saccharomyces cerevisiae, a double lipid bilayer called the prospore membrane is formed de novo, growing around each meiotic nucleus and ultimately closing to create four new cells within the mother cell. Here we show that SPS1, which encodes a kinase belonging to the germinal center kinase III family, is involved in prospore membrane development and is required for prospore membrane closure. We find that SPS1 genetically interacts with SPO77 and see that loss of either gene disrupts prospore membrane closure in a similar fashion. Specifically, cells lacking SPS1 and SPO77 produce hyperelongated prospore membranes from which the leading edge protein complex is not removed from the prospore membrane in a timely fashion. The SPS1/ SPO77 pathway is required for the proper phosphorylation and stability of Ssp1, a member of the leading edge protein complex that is removed and degraded when the prospore membrane closes. Genetic dissection of prospore membrane closure finds SPS1 and SPO77 act in parallel to a previously described pathway of prospore membrane closure that involves AMA1, an activator of the meiotic anaphase promoting complex.KEYWORDS prospore membrane; meiotic exit; anaphase promoting complex; sporulation; cytokinesis; germinal center kinase B IOLOGICAL membranes provide a barrier for inhibiting the flow of materials between a cell and its surroundings and for compartmentalizing the contents of the various organelles within a cell. The size and shape of membranes are central to their functions. Membranes are essential for many fundamental cellular processes including ion balance, energy generation, and secretion. In cell division, membrane dynamics are particularly important, where they act to segregate the contents of the cellular progeny.The process of cell division differs among cells. Most commonly, animal cells divide through a mechanism requiring the assembly of an actin-based contractile ring at the division site (reviewed in Green et al. 2012). This actomyosin ring contracts and matures, ultimately leading to scission of the membrane necks mediated by the ESCRTIII (endosomal sorting complex required for transport III) complex. However, other variations of cytokinesis occur: cellularization during early Drosophila embryogenesis, which requires the growth of membranes around the nuclei before the contractile event (Lee and Harris 2014) and cell division in plants, which requires the secretion of vesicles to the division plane to form the phragmoplast, which will eventually separate the two daughter cells (reviewed in Jürgens 2005). Actin is not always involved in cytokinesis; although prokaryotic cells have actin-like filaments (reviewed in Carballido-López 2006), these filaments are not used for cytokinesis (Pollard and Wu 2010). Similarly, cytokinesis in Trypanosoma brucei (a bikont eukaryote) does not require actin but seems to utilize microtubules (Wheeler et al. 2013). In the budding yeast Saccharomyces cerevisiae, an actin-based contractile ring plays a role in ...

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Timely Closure of the Prospore Membrane Requires SPS1 and SPO77 in Saccharomyces cerevisiae

et al. 2016

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“…Colony sporulation patterns may reflect differences in nutrient environment across the community as well as cell-to-cell signals within communities [reviewed in Honigberg (2011)]. One function of sporulation patterning may be to localize sporulated cells to the surfaces of colonies to maximize their dispersal; spores are resistant to environmental stress and may be largely dispersed by insect vectors that feed at the surfaces of these microbial communities [reviewed in Neiman (2011)]. A second possible function of sporulation patterning is to efficiently distribute limited nutrients within the community.…”

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Cell Differentiation and Spatial Organization in Yeast Colonies: Role of Cell-Wall Integrity Pathway

Piccirillo¹,

Morales²,

White³

et al. 2015

Genetics

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Many microbial communities contain organized patterns of cell types, yet relatively little is known about the mechanism or function of this organization. In colonies of the budding yeast Saccharomyces cerevisiae, sporulation occurs in a highly organized pattern, with a top layer of sporulating cells sharply separated from an underlying layer of nonsporulating cells. A mutant screen identified the Mpk1 and Bck1 kinases of the cell-wall integrity (CWI) pathway as specifically required for sporulation in colonies. The CWI pathway was induced as colonies matured, and a target of this pathway, the Rlm1 transcription factor, was activated specifically in the nonsporulating cell layer, here termed feeder cells. Rlm1 stimulates permeabilization of feeder cells and promotes sporulation in an overlying cell layer through a cell-nonautonomous mechanism. The relative fraction of the colony apportioned to feeder cells depends on nutrient environment, potentially buffering sexual reproduction against suboptimal environments.KEYWORDS cell-wall integrity; cell permeability; cell-cell signaling; Saccharomyces cerevisiae; sporulation A S embryos develop, cells of different fates organize into patterns [reviewed in Kicheva et al. (2012) and Perrimon et al. (2012)] . Intriguingly, even unicellular microbial species form communities in which different cell types are organized into patterns [reviewed in Kaiser et al. (2010), Honigberg (2011, and Loomis (2014)]. For example, colonies of the budding yeast Saccharomyces cerevisiae form an upper layer of larger cells (U cells) overlying a layer of smaller cells (L cells). U and L cells differ in their metabolism, gene expression, and resistance to stress, and U and L layers are separated by a strikingly sharp boundary Vachova et al. 2013). Patterns are also observed in yeast biofilms, where cells closest to the plastic surface grow as ovoid cells, whereas cells further from the surface differentiate into hyphae for Candida species [reviewed in Finkel and Mitchell (2011)] or pseudohyphae and eventually asci for S. cerevisiae (White et al. 2011).Sporulation also occurs in patterns within yeast colonies. Specifically, a narrow horizontal layer of sporulated cells forms through the center of the colony early during colony development. As colonies continue to mature, this layer progressively expands upward to include the top of the colony; this wave is driven by progressive alkalization and activation of the Rim101 signaling pathway . In contrast, cells at the bottom of the colony, i.e., directly contacting the agar substrate, also sporulate at early stages of colony development, but this narrow cell layer does not expand as the colony matures . The same colony sporulation pattern is observed in a range of laboratory yeasts as well as in S. cerevisiae and S. paradoxus isolated from the wild. Indeed, in these wild yeasts, the same colony sporulation pattern forms on a range of fermentable and nonfermentable carbon sources .The mechanism of sporulation patterning and its function remai...

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“…Haploid yeast undergoes morphological changes in response to secreted pheromones to mate and form diploids (Bardwell 2005;Dohlman and Slessareva 2006;Merlini et al 2013). Diploid yeast starved for carbon and nitrogen initiate a meiotic program known as sporulation (Neiman 2011). Haploid and diploid yeast starved for only carbon or nitrogen undergoes filamentous (or invasive/pseudohyphal) growth (Gimeno et al 1992;Sprague 2000, 2012).…”

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Global Regulation of a Differentiation MAPK Pathway in Yeast

Chavel

Caccamise

Li³

et al. 2014

Genetics

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Cell differentiation requires different pathways to act in concert to produce a specialized cell type. The budding yeast Saccharomyces cerevisiae undergoes filamentous growth in response to nutrient limitation. Differentiation to the filamentous cell type requires multiple signaling pathways, including a mitogen-activated protein kinase (MAPK) pathway. To identify new regulators of the filamentous growth MAPK pathway, a genetic screen was performed with a collection of 4072 nonessential deletion mutants constructed in the filamentous (S1278b) strain background. The screen, in combination with directed gene-deletion analysis, uncovered 97 new regulators of the filamentous growth MAPK pathway comprising 40% of the major regulators of filamentous growth. Functional classification extended known connections to the pathway and identified new connections. One function for the extensive regulatory network was to adjust the activity of the filamentous growth MAPK pathway to the activity of other pathways that regulate the response. In support of this idea, an unregulated filamentous growth MAPK pathway led to an uncoordinated response. Many of the pathways that regulate filamentous growth also regulated each other's targets, which brings to light an integrated signaling network that regulates the differentiation response. The regulatory network characterized here provides a template for understanding MAPK-dependent differentiation that may extend to other systems, including fungal pathogens and metazoans.

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Sporulation in the Budding Yeast Saccharomyces cerevisiae

Cited by 350 publications

References 293 publications

Timely Closure of the Prospore Membrane Requires SPS1 and SPO77 in Saccharomyces cerevisiae

Timely Closure of the Prospore Membrane Requires SPS1 and SPO77 in Saccharomyces cerevisiae

Cell Differentiation and Spatial Organization in Yeast Colonies: Role of Cell-Wall Integrity Pathway

Global Regulation of a Differentiation MAPK Pathway in Yeast

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