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  • Review Article
  • Published:

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

An Erratum to this article was published on 01 January 2009

Key Points

  • 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.

Abstract

Organisms are constantly exposed to a wide range of environmental changes, including both short-term changes during their lifetime and longer-term changes across generations. Stress-related gene expression programmes, characterized by distinct transcriptional mechanisms and high levels of noise in their expression patterns, need to be balanced with growth-related gene expression programmes. A range of recent studies give fascinating insight into cellular strategies for keeping gene expression in tune with physiological needs dictated by the environment, promoting adaptation to both short- and long-term environmental changes. Not only do organisms show great resilience to external challenges, but emerging data suggest that they also exploit these challenges to fuel phenotypic variation and evolutionary innovation.

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Figure 1: Balancing the expression of growth- and stress-related genes.
Figure 2: Stress- and growth-related genes show distinct regulatory features.
Figure 3: Synthetic regulatory circuits to study responses to unknown challenges.

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Acknowledgements

We apologize to colleagues in the field for not citing all relevant papers owing to space constraints. We thank C. Wilkinson, J. Mata, D. Lackner, V. Pancaldi and F. Schubert for comments on the manuscript. Research in our laboratory is supported by Cancer Research UK. L.L.-M. and S.M. are supported by postdoctoral fellowships from FEBS and the Swiss National Science Foundation, respectively.

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Correspondence to Jürg Bähler.

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Glossary

Core stress response

Involves genes with expression levels that are regulated in a stereotypical manner in all (or most) of the environmental stress conditions tested in yeasts. This response is also known as the environmental stress response (ESR), common environmental response (CER) or core environmental stress response (CESR).

Chemostat

A fermenter that is operated in continuous-culture mode and is used in microbiology for growing and harvesting microorganisms at defined growth rates and under tightly controlled conditions.

TFIID

A complex that is composed of TBP and TAFs. Binding of TFIID to DNA is necessary but not sufficient for transcription initiation from most promoters.

SAGA

A large multi-protein complex involved in the regulation of transcription that possesses histone acetyltransferase and TBP-binding activities. The budding-yeast complex includes Gcn5, several proteins of the Spt and Ada families, and several TAFs; analogous complexes in other species have analogous compositions, and usually contain homologues of the yeast proteins.

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López-Maury, L., Marguerat, S. & Bähler, J. Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet 9, 583–593 (2008). https://doi.org/10.1038/nrg2398

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