Phenotypic plasticity within yeast colonies: differential partitioning of cell fates

Abstract

Across many phyla, a common aspect of multicellularity is the organization of different cell types into spatial patterns. In the budding yeast Saccharomyces cerevisiae, after diploid colonies have completed growth, they differentiate to form alternating layers of sporulating cells and feeder cells. In the current study, we found that as yeast colonies developed, the feeder cell layer was initially separated from the sporulating cell layer. Furthermore, the spatial pattern of sporulation in colonies depended on the colony's nutrient environment; in two environments in which overall colony sporulation efficiency was very similar, the pattern of feeder and sporulating cells within the colony was very different. As noted previously, under moderately suboptimal conditions for sporulation-low acetate concentration or high temperature-the number of feeder cells increases as does the dependence of sporulation on the feeder-cell transcription factor, Rlm1. Here we report that even under a condition that is completely blocked sporulation, the number of feeder cells still increased. These results suggest broader implications to our recently proposed "Differential Partitioning provides Environmental Buffering" or DPEB hypothesis.

Keywords: Allocation; Cell-wall integrity; IME2; Meiosis; Quiescent; RLM1.

Fig. 1. Confocal image of PI-permeability and ime2Δ-GFP expression in colonies

Colonies of strain SH4793 were grown for 4 d, stained with PI, and visualized by confocal microscopy.. Section shown is through the center of the colony, with the top of the colony at the top of the image. Red cells = PI, green cells= ime2Δ-GFP expression. PI and GFP images were collected separately and then merged (Image J). Scale bar = 50 μ.

Fig. 2. Sections of yeast colonies grown on different concentrations of nitrogen source

A) Sections of two colonies grown on YA medium (0.5% yeast extract) for 10 d, B) Distribution of sporulated cells in colonies grown as in A) determined by superimposing a grid containing nine equal-sized rectangles stacked on top of one another (long side horizontal) on each image scaled to just cover central region of colony from bottom to top. Distributions show percentage of the population recognized as asci in each of these rectangles from the top (T, left) to bottom (B, right) of the colony. C) Sections of two colonies grown on LYA medium (0.25% yeast extract) for 10 d. D) Distribution of sporulated cells in colonies grown as in C) determined as described in B). Scale bars in (A) and (C) are 50 μ. Error bars in (B) and (D) represent SEM, n=3.

Fig. 3. Effect of acetate concentrations and temperature on the fraction of sporulating and feeder cells in colonies and dependence of sporulation on RLM1

A) Fraction of colony (SH3881) that formed spores at indicated potassium acetate concentrations (x-axis) and temperature (y-axis). B) Fraction of colonies under same conditions as in A) identifiable as feeder cells by expression of the UAS_Rlm1-LacZ allele in strain SH5065. C) Dependence of colony sporulation on RLM1 grown under the same conditions as in (A). Dependence score = sporulation frequency in RLM1 colony (SH3881)/sporulation frequency in rlm1Δ colony (SH4708). Error bars are SEM, n = 3.