Cells show a remarkable regulatory flexibility that allows
them to thrive under different external conditions and
to survive harsh situations. The ability to constantly
sense and adapt to environmental changes is important
for all organisms to maintain cellular functions (home-
ostasis), but is especially acute for plants and microor-
ganisms; their sessile lifestyle leave them more exposed
to the environment than animals. Modulation of gene
expression has a central role in cellular adaptation to
short- or long-term environmental changes, with exten-
sive regulation occurring at both the transcriptional and
post-transcriptional level. Signal-transduction pathways
can translate extracellular signals into specific intracel-
lular responses, including the launch of alternative gene
expression programmes to cope with new conditions. In
addition to these ‘hard-wired’ responses, gene expres-
sion networks show considerable plasticity to adapt to
a wide range of challenges, including those not encoun-
tered during evolutionary history (for example, ectopic
gene expression).
The application of genome-wide approaches is now
providing a global view on gene expression responses
to many different stress conditions, leading to exciting
recent advances in our understanding of the cellular
strategies that are used to stay in tune with environ-
mental conditions. Many of these concepts have been
developed in microorganisms, most notably yeast cells,
which finely balance energy-efficient growth with the
ability to rapidly adapt to sudden external challenges,
and which provide ideal models to study gene expres-
sion under tightly controlled conditions. Research in
yeast and in other organisms is uncovering conserved
principles for regulatory strategies in response to chang-
ing environments. This Review will highlight some of
the emerging principles underlying gene expression
responses to environmental factors. The emphasis
will be on transcriptional mechanisms, which have
been most intensely studied for technical and histori-
cal reasons, and for which several recent papers have
greatly advanced our understanding. The details of
regulatory pathways or specific cellular responses to
different stresses have been reviewed elsewhere
1–4
. We
focus on the general principles by which cells are able to
adjust their gene expression programmes to respond
to changing environments, both in the short-term and
over evolutionary timescales. Emerging data reveal
that cells finely balance the expression of stress-related
and growth-related genes, which are antagonistic pro-
grammes distinguished by distinct regulatory mecha-
nisms. Stress-related genes generally contain TATA
boxes, a promoter element that seems to promote both
short-term variability and long-term evolvability of
transcriptional responses. Maintaining cellular func-
tionality under variable conditions thus enhances gene
expression variability and is both a constraint and a
driving force for evolution.
Department of Genetics,
Evolution and Environment,
and UCL Cancer Institute,
University College London,
London WC1E 6BT, UK.
Correspondence to J.B.
e-mail: jurg@sanger.ac.uk
doi:10.1038/nrg2398
Published online 1 July 2008
Tuning gene expression to changing
environments: from rapid responses
to evolutionary adaptation
Luis López-Maury, Samuel Marguerat and Jürg Bähler
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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