Cells must adjust their
gene expression in order to compete in a constantly changing environment. Two alternative strategies could in principle ensure optimal coordination of
gene expression with physiological requirements. First, characters of the internal physiological state, such as growth rate,
metabolite levels, or energy availability, could be feedback to tune
gene expression. Second, internal needs could be
inferred from the external environment, using evolutionary-tuned
signaling pathways. Coordination of
ribosomal biogenesis with the requirement for
protein synthesis is of particular importance, since cells devote a large fraction of their biosynthetic capacity for
ribosomal biogenesis. To define the relative contribution of internal vs. external sensing to the regulation of
ribosomal biogenesis
gene expression in
yeast, we subjected
S. cerevisiae cells to 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 during
yeast evolution.
