Abstract: When a cell encounters a new environment, its transcriptional response can be constrained by its history. For example, yeast cells in galactose induce GAL genes with a speed and unanimity that depends on previous nutrient conditions. Cellular memory of long-term glucose exposure delays GAL induction and makes it highly variable with in a cell population, while other nutrient histories lead to rapid, uniform responses. To investigate how cell-level gene expression dynamics produce population-level phenotypes, we collected thousands of microscopy images of fields of cells as they switched to galactose from various nutrient histories, extracted time series of thousands of individual cells undergoing this shift, and used these to build living vector fields as the cells moved across the state space of the proteins Gal3p and Gal1p. We show that, after sustained glucose exposure, the lack of these GAL transducers leads to induction delays that are long but also variable; that cellular resources constrain induction; and that bimodally distributed expression levels arise from lineage selection - a subpopulation of cells induces more quickly and outcompetes the rest. Our results illuminate cellular memory in this important model system and illustrate how resources and randomness interact to shape the response of a population to a new environment.
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