Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation

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Abstract
Cells show a remarkable resilience that allows them to thrive under different external conditions and to survive harsh situations. Gene regulation has a central role in cellular adaptation to both short- and long-term environmental changes. Recent studies provide exciting advances in our understanding of cellular strategies to stay in tune with environmental fluctuations, most notably at the transcriptional level of control. Many of these concepts have been developed in microorganisms such as yeast, which finely balance energy-efficient growth with the ability to rapidly respond to sudden external challenges. Global expression of stress- and growth-related genes is finely balanced in yeast, reflecting antagonistic programmes that are controlled by different signalling pathways and transcriptional mechanisms. The balance of cellular growth versus stress is highly regulated at the level of general transcription factors. Yeast have a bipolar transcriptome, in terms of distinct types of core promoters that are used to control growth- or stress-related genes. Stress-related genes generally contain a TATA box — a promoter element that not only promotes variability (that is, noise) in short-term transcriptional responses but also promotes regulatory divergence during evolution. Core promoter-complex switching, which allows the selective activation of one transcriptional programme while silencing others during mammalian differentiation, is reminiscent of the mechanism used by yeast to control growth- versus stress-related genes. Maintaining cellular functionality under variable conditions enhances gene expression variability and is both a constraint and a driving force for evolution. Phenotypic heterogeneity caused by gene expression variability increases survival in fluctuating environments. In addition to hard-wired regulatory responses, gene expression networks show a remarkable plasticity to adapt to a wide range of unpredictable conditions, including those not encountered during evolutionary history.