scholarly journals Multicellular Group Formation in Saccharomyces cerevisiae

Author(s):  
Roberta Fisher ◽  
Birgitte Regenberg

Understanding how and why cells cooperate to form multicellular organisms is a central aim of evolutionary biology. Multicellular groups can form through clonal development (where daughter cells stick to mother cells after division) or by aggregation (where cells aggregate to form groups). These different ways of forming groups directly affect relatedness between individual cells, which in turn influences the degree of cooperation and conflict within the multicellular group. It is hard to study the factors that favoured multicellularity by focusing only on obligately multicellular organisms, like complex animals and plants, because the factors that favour multicellular cooperation cannot be disentangled, as cells cannot survive and reproduce independently. We propose bakers yeast, Saccharomyces cerevisiae, as an ideal model for studying the very first stages of the evolution of multicellularity. This is because it can form multicellular groups both clonally and through aggregation and uses a family of proteins called ‘flocculins’ that determine the way in which groups form, making it particularly amenable to lab experiments. We briefly review current knowledge about multicellularity in S. cerevisiae and then propose a framework for making predictions about the evolution of multicellular phenotypes in yeast based on social evolution theory. We finish by suggesting outstanding questions and potentially fruitful avenues for future research.

2019 ◽  
Vol 286 (1910) ◽  
pp. 20191098 ◽  
Author(s):  
R. M. Fisher ◽  
B. Regenberg

Understanding how and why cells cooperate to form multicellular organisms is a central aim of evolutionary biology. Multicellular groups can form through clonal development (where daughter cells stick to mother cells after division) or by aggregation (where cells aggregate to form groups). These different ways of forming groups directly affect relatedness between individual cells, which in turn can influence the degree of cooperation and conflict within the multicellular group. It is hard to study the evolution of multicellularity by focusing only on obligately multicellular organisms, like complex animals and plants, because the factors that favour multicellular cooperation cannot be disentangled, as cells cannot survive and reproduce independently. We support the use of Saccharomyces cerevisiae as an ideal model for studying the very first stages of the evolution of multicellularity. This is because it can form multicellular groups both clonally and through aggregation and uses a family of proteins called ‘flocculins’ that determine the way in which groups form, making it particularly amenable to laboratory experiments. We briefly review current knowledge about multicellularity in S. cerevisiae and then propose a framework for making predictions about the evolution of multicellular phenotypes in yeast based on social evolution theory. We finish by explaining how S. cerevisiae is a particularly useful experimental model for the analysis of open questions concerning multicellularity.


Genes ◽  
2020 ◽  
Vol 11 (6) ◽  
pp. 690 ◽  
Author(s):  
Monika Opalek ◽  
Dominika Wloch-Salamon

The evolutionary transition from single-celled to multicellular growth is a classic and intriguing problem in biology. Saccharomyces cerevisiae is a useful model to study questions regarding cell aggregation, heterogeneity and cooperation. In this review, we discuss scenarios of group formation and how this promotes facultative multicellularity in S. cerevisiae. We first describe proximate mechanisms leading to aggregation. These mechanisms include staying together and coming together, and can lead to group heterogeneity. Heterogeneity is promoted by nutrient limitation, structured environments and aging. We then characterize the evolutionary benefits and costs of facultative multicellularity in yeast. We summarize current knowledge and focus on the newest state-of-the-art discoveries that will fuel future research programmes aiming to understand facultative microbial multicellularity.


1994 ◽  
Vol 127 (6) ◽  
pp. 1985-1993 ◽  
Author(s):  
B K Kennedy ◽  
N R Austriaco ◽  
L Guarente

The yeast Saccharomyces cerevisiae typically divides asymmetrically to give a large mother cell and a smaller daughter cell. As mother cells become old, they enlarge and produce daughter cells that are larger than daughters derived from young mother cells. We found that occasional daughter cells were indistinguishable in size from their mothers, giving rise to a symmetric division. The frequency of symmetric divisions became greater as mother cells aged and reached a maximum occurrence of 30% in mothers undergoing their last cell division. Symmetric divisions occurred similarly in rad9 and ste12 mutants. Strikingly, daughters from old mothers, whether they arose from symmetric divisions or not, displayed reduced life spans relative to daughters from young mothers. Because daughters from old mothers were larger than daughters from young mothers, we investigated whether an increased size per se shortened life span and found that it did not. These findings are consistent with a model for aging that invokes a senescence substance which accumulates in old mother cells and is inherited by their daughters.


1984 ◽  
Vol 4 (11) ◽  
pp. 2529-2531 ◽  
Author(s):  
B J Brewer ◽  
E Chlebowicz-Sledziewska ◽  
W L Fangman

During cell division in the yeast Saccharomyces cerevisiae mother cells produce buds (daughter cells) which are smaller and have longer cell cycles. We performed experiments to compare the lengths of cell cycle phases in mothers and daughters. As anticipated from earlier indirect observations, the longer cell cycle time of daughter cells is accounted for by a longer G1 interval. The S-phase and the G2-phase are of the same duration in mother and daughter cells. An analysis of five isogenic strains shows that cell cycle phase lengths are independent of cell ploidy and mating type.


2020 ◽  
Vol 287 (1931) ◽  
pp. 20192963
Author(s):  
R. M. Fisher ◽  
J. Z. Shik ◽  
J. J. Boomsma

A major challenge in evolutionary biology has been to explain the variation in multicellularity across the many independently evolved multicellular lineages, from slime moulds to vertebrates. Social evolution theory has highlighted the key role of relatedness in determining multicellular complexity and obligateness; however, there is a need to extend this to a broader perspective incorporating the role of the environment. In this paper, we formally test Bonner's 1998 hypothesis that the environment is crucial in determining the course of multicellular evolution, with aggregative multicellularity evolving more frequently on land and clonal multicellularity more frequently in water. Using a combination of scaling theory and phylogenetic comparative analyses, we describe multicellular organizational complexity across 139 species spanning 14 independent transitions to multicellularity and investigate the role of the environment in determining multicellular group formation and in imposing constraints on multicellular evolution. Our results, showing that the physical environment has impacted the way in which multicellular groups form, highlight that environmental conditions might have affected the major evolutionary transition to obligate multicellularity.


1999 ◽  
Vol 145 (6) ◽  
pp. 1177-1188 ◽  
Author(s):  
Sylvia L. Sanders ◽  
Martina Gentzsch ◽  
Widmar Tanner ◽  
Ira Herskowitz

Cells of the yeast Saccharomyces cerevisiae choose bud sites in a manner that is dependent upon cell type: a and α cells select axial sites; a/α cells utilize bipolar sites. Mutants specifically defective in axial budding were isolated from an α strain using pseudohyphal growth as an assay. We found that a and α mutants defective in the previously identified PMT4 gene exhibit unipolar, rather than axial budding: mother cells choose axial bud sites, but daughter cells do not. PMT4 encodes a protein mannosyl transferase (pmt) required for O-linked glycosylation of some secretory and cell surface proteins (Immervoll, T., M. Gentzsch, and W. Tanner. 1995. Yeast. 11:1345–1351). We demonstrate that Axl2/Bud10p, which is required for the axial budding pattern, is an O-linked glycoprotein and is incompletely glycosylated, unstable, and mislocalized in cells lacking PMT4. Overexpression of AXL2 can partially restore proper bud-site selection to pmt4 mutants. These data indicate that Axl2/Bud10p is glycosylated by Pmt4p and that O-linked glycosylation increases Axl2/ Bud10p activity in daughter cells, apparently by enhancing its stability and promoting its localization to the plasma membrane.


2001 ◽  
Vol 48 (4) ◽  
pp. 1025-1042 ◽  
Author(s):  
R Kucharczyk ◽  
J Rytka

The role of the yeast vacuole, a functional analogue of the mammalian lysosome, in the turnover of proteins and organelles has been well documented. This review provides an overview of the current knowledge of vesicle mediated vacuolar transport in the yeast Saccharomyces cerevisiae cells. Due to the conservation of the molecular transport machinery S. cerevisiae has become an important model system of vacuolar trafficking because of the facile application of genetics, molecular biology and biochemistry.


1995 ◽  
Vol 129 (3) ◽  
pp. 751-765 ◽  
Author(s):  
J Chant ◽  
J R Pringle

Cells of the yeast Saccharomyces cerevisiae select bud sites in either of two distinct spatial patterns, known as axial (expressed by a and alpha cells) and bipolar (expressed by a/alpha cells). Fluorescence, time-lapse, and scanning electron microscopy have been used to obtain more precise descriptions of these patterns. From these descriptions, we conclude that in the axial pattern, the new bud forms directly adjacent to the division site in daughter cells and directly adjacent to the immediately preceding division site (bud site) in mother cells, with little influence from earlier sites. Thus, the division site appears to be marked by a spatial signal(s) that specifies the location of the new bud site and is transient in that it only lasts from one budding event to the next. Consistent with this conclusion, starvation and refeeding of axially budding cells results in the formation of new buds at nonaxial sites. In contrast, in bipolar budding cells, both poles are specified persistently as potential bud sites, as shown by the observations that a pole remains competent for budding even after several generations of nonuse and that the poles continue to be used for budding after starvation and refeeding. It appears that the specification of the two poles as potential bud sites occurs before a daughter cell forms its first bud, as a daughter can form this bud near either pole. However, there is a bias towards use of the pole distal to the division site. The strength of this bias varies from strain to strain, is affected by growth conditions, and diminishes in successive cell cycles. The first bud that forms near the distal pole appears to form at the very tip of the cell, whereas the first bud that forms near the pole proximal to the original division site (as marked by the birth scar) is generally somewhat offset from the tip and adjacent to (or overlapping) the birth scar. Subsequent buds can form near either pole and appear almost always to be adjacent either to the birth scar or to a previous bud site. These observations suggest that the distal tip of the cell and each division site carry persistent signals that can direct the selection of a bud site in any subsequent cell cycle.


2002 ◽  
Vol 13 (12) ◽  
pp. 4141-4155 ◽  
Author(s):  
Marisa Segal ◽  
Kerry Bloom ◽  
Steven I. Reed

Spindle orientation is critical for accurate chromosomal segregation in eukaryotic cells. In the yeast Saccharomyces cerevisiae, orientation of the mitotic spindle is achieved by a program of microtubule–cortex interactions coupled to spindle morphogenesis. We previously implicated Bud6p in directing microtubule capture throughout this program. Herein, we have analyzed cells coexpressing GFP:Bud6 and GFP:Tub1 fusions, providing a kinetic view of Bud6p–microtubule interactions in live cells. Surprisingly, even during the G1 phase, microtubule capture at the recent division site and the incipient bud is dictated by Bud6p. These contacts are eliminated in bud6Δ cells but are proficient inkar9Δ cells. Thus, Bud6p cues microtubule capture, as soon as a new cell polarity axis is established independent of Kar9p. Bud6p increases the duration of interactions and promotes distinct modes of cortical association within the bud and neck regions. In particular, microtubule shrinkage and growth at the cortex rarely occur away from Bud6p sites. These are the interactions selectively impaired at the bud cortex in bud6Δ cells. Finally, interactions away from Bud6p sites within the bud differ from those occurring at the mother cell cortex, pointing to the existence of an independent factor controlling cortical contacts in mother cells after bud emergence.


2019 ◽  
Author(s):  
RM Fisher ◽  
JZ Shik ◽  
JJ Boomsma

AbstractA major challenge in evolutionary biology has been to explain the variation in multicellularity across the many independently evolved multicellular lineages, from slime moulds to humans. Social evolution theory has highlighted the key role of relatedness in determining multicellular complexity and obligateness, however there is a need to extend this to a broader perspective incorporating the role of the environment. In this paper, we formally test Bonner’s 1998 hypothesis that the environment is crucial in determining the course of multicellular evolution, with aggregative multicellularity evolving more frequently on land and clonal multicellularity more frequently in water. Using a combination of scaling theory and phylogenetic comparative analyses, we describe multicellular organisational complexity across 139 species spanning 14 independent transitions to multicellularity and investigate the role of the environment in determining multicellular group formation and in imposing constraints on multicellular evolution. Our results, showing that the physical environment has impacted the way in which multicellular groups form, could shed light on the role of the environment for other major evolutionary transitions.


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