The relative contribution of 'internal' vs. 'external' sensing to the regulation of gene expression in the budding yeast

Abstract

Cells monitor their external environment using membrane receptors, modulating their gene expression pattern in response to external cues. In addition, cells monitor the level of internal metabolites, energy availability, and growth rate, and these internal characters also feedback to tune gene expression. We examined the relative contribution of internal vs. external sensing to the regulation of ribosomal biogenesis gene expression in yeast. Since cells devote a large fraction of their biosynthetic capacity for ribosomal biogenesis, coordination of ribosomal biogenesis with the requirement for protein synthesis is of particular importance. To distinguish between 'external' and 'internal' sensing, we subjected S. cerevisiae cells to 'confusing' conditions which decoupled the actual vs. environmentally‐expected growth rate. Gene expression followed the environmental signal according to the expected, but not the actual, growth rate. Simultaneous monitoring of gene expression and growth rate in continuous cultures further confirmed that ribosome biogenesis genes responded rapidly to changes in the environments but were oblivious to longer‐term changes in growth rate. Our results suggest that the capacity to anticipate and prepare for environmentally‐mediated changes in cell growth presented a major selection force in the evolution of yeast, and perhaps also of other micro‐organisms.