© 2012 Nature America, Inc. All rights reserved.
NATURE GENETICS ADVANCE ONLINE PUBLICATION 1
ARTICLES
Precise regulation of expression is vital to most biological functions.
A key challenge is to unravel how this regulation is encoded within
genomes and to be able to understand, predict and design expres-
sion patterns from regulatory sequences. Addressing this challenge
requires knowledge of both the functional elements within regulatory
sequences and the ways in which such elements combine to specify
regulatory programs. Much of the research in the field has focused on
the role of transcription factors and their binding sites
1
. Despite much
progress, our ability to understand transcriptional regulation using
only transcription factors remains limited. Recent studies suggested
that nucleosome organization of regulatory regions is essential for
bridging this gap. Because transcription factor–binding sites that are
wrapped into nucleosomes are less accessible to binding by their cog-
nate factor compared to sites located in nucleosome-free regions
2,3
,
we expect that the transcriptional output directed by the same site
will depend on its surrounding nucleosome organization
4–7
.
A strong determinant of nucleosome organization is the presence of
homopolymeric stretches of deoxyadenosine nucleotides, referred to
as poly(dA:dT) tracts. These sequence elements disfavor nucleosome
formation
8,9
and are strongly associated with nucleosome depletion
over the tract itself and its surrounding DNA in both in vivo
10,11
and in vitro
10,12
genome-wide studies. Notably, these tracts are highly
abundant in eukaryotic genomes
13
and are particularly prevalent in
promoters
14
. Consistent with these observations and with a role for
nucleosome organization in determining transcriptional output, a study
that altered the presence and length of a native poly(dA:dT) element
in one yeast promoter showed that this tract can indeed stimulate
expression, most likely by conferring increased accessibility to the
nearby transcription factor–binding site
15
. Thus, sequences that
strongly disfavor nucleosome formation may also serve as important
promoter building blocks.
Despite this potentially important regulatory role of poly(dA:dT)
tracts, very little is known about the extent and nature of their tran-
scriptional effect. What is the magnitude of their effect compared to
that of other regulatory elements? How does their effect depend on
their own sequence properties and on properties of other regulatory
elements such as the affinity of nearby transcription factor sites? And
how does the overall arrangement of these tracts and other regulatory
elements determine the transcriptional output?
Here, we systematically address the above questions by measur-
ing the activities of 70 different promoter variants that we designed
with poly(dA:dT) tracts that differ in their length, composition and
distance from several distinct transcription factor sites. We further
characterize the transcriptional effect of poly(dA:dT) tracts by nucleo-
some occupancy and single-cell expression measurements. Notably,
we show that, by manipulating only poly(dA:dT) tracts, we can affect
nucleosome organization and predictably alter the resulting tran-
scriptional level to a significant extent, comparable to that attained
by altering transcription factor sites. In fact, compared to binding
site alterations, poly(dA:dT) manipulations can yield more gradual
changes and may thus offer a genetic mechanism by which expression
can be tuned with finer resolution.
Manipulating nucleosome disfavoring sequences allows
fine-tune regulation of gene expression in yeast
Tali Raveh-Sadka
1,2,4
, Michal Levo
1,2,4
, Uri Shabi
3
, Boaz Shany
1,2
, Leeat Keren
1,2
, Maya Lotan-Pompan
1,2
,
Danny Zeevi
1,2
, Eilon Sharon
1,2
, Adina Weinberger
1,2
& Eran Segal
1,2
Understanding how precise control of gene expression is specified within regulatory DNA sequences is a key challenge with
far-reaching implications. Many studies have focused on the regulatory role of transcription factor–binding sites. Here,
we explore the transcriptional effects of different elements, nucleosome-disfavoring sequences and, specifically, poly(dA:dT)
tracts that are highly prevalent in eukaryotic promoters. By measuring promoter activity for a large-scale promoter library,
designed with systematic manipulations to the properties and spatial arrangement of poly(dA:dT) tracts, we show that these
tracts significantly and causally affect transcription. We show that manipulating these elements offers a general genetic
mechanism, applicable to promoters regulated by different transcription factors, for tuning expression in a predictable manner,
with resolution that can be even finer than that attained by altering transcription factor sites. Overall, our results advance the
understanding of the regulatory code and suggest a potential mechanism by which promoters yielding prespecified expression
patterns can be designed.
1
Department of Computer Science and Applied Mathematics, Weizmann Institute of Science, Rehovot, Israel.
2
Department of Molecular Cell Biology, Weizmann
Institute of Science, Rehovot, Israel.
3
Department of Biological Chemistry, Weizmann Institute of Science, Rehovot, Israel.
4
These authors contributed equally to this
work. Correspondence should be addressed to E.S. (eran.segal@weizmann.ac.il) or A.W. (adina.weinberger@weizmann.ac.il).
Received 26 January; accepted 3 May; published online 27 May 2012; doi:10.1038/ng.2305