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A genetic signature of interspecies variations in gene expression

Nature Genetics volume 38, pages 830–834 (2006)Cite this article

Abstract

Phenotypic diversity is generated through changes in gene structure or gene regulation. The availability of full genomic sequences allows for the analysis of gene sequence evolution. In contrast, little is known about the principles driving the evolution of gene expression. Here we describe the differential transcriptional response of four closely related yeast species to a variety of environmental stresses. Genes containing a TATA box in their promoters show an increased interspecies variability in expression, independent of their functional association. Examining additional data sets, we find that this enhanced expression divergence of TATA-containing genes is consistent across all eukaryotes studied to date, including nematodes, fruit flies, plants and mammals. TATA-dependent regulation may enhance the sensitivity of gene expression to genetic perturbations, thus facilitating expression divergence at particular genetic loci.

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Figure 1: Experimental design.
Figure 2: The TATA box is associated with high expression divergence.
Figure 3: TATA-containing genes are associated with high expression divergence in various data sets.
Figure 4: Properties of TATA-containing promoters.

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Acknowledgements

We thank A. Koren, A. Murray, J. Plotkin and members of our laboratory for helpful discussions. This work was supported by a grant from the Kahn Fund for Systems Biology at the Weizmann Institute of Science and by the Israeli Ministry of Science (Tashtiot). N.B. acknowledges the Bauer Center for Genomic Research at Harvard University, where part of this research was performed.

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Author notes

  1. Itay Tirosh and Adina Weinberger: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, 76100, Israel

    Itay Tirosh, Adina Weinberger, Miri Carmi & Naama Barkai

  2. Department of Physics of Complex Systems, Weizmann Institute of Science, Rehovot, 76100, Israel

    Naama Barkai

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  1. Itay Tirosh
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  2. Adina Weinberger
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  3. Miri Carmi
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Corresponding author

Correspondence to Naama Barkai.

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Supplementary information

Supplementary Fig. 1

Cross-species hybridization control. (PDF 243 kb)

Supplementary Fig. 2

Expression divergence controls. (PDF 102 kb)

Supplementary Fig. 3

TATA-ED association within functional groups, for different classes of hybridization intensities. (PDF 88 kb)

Supplementary Fig. 4

TATA-ED association within functional groups, in different data sets. (PDF 84 kb)

Supplementary Fig. 5

SAGA/TFIID dependency and the histone variant Htz1 can partially account for the increased expression divergence of TATA-containing genes. (PDF 74 kb)

Supplementary Fig. 6

Enrichment of TATA boxes in functional categories in yeast and humans. (PDF 86 kb)

Supplementary Table 1

TATA box versus expression divergence in various data sets. (PDF 72 kb)

Supplementary Methods (PDF 296 kb)

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Tirosh, I., Weinberger, A., Carmi, M. et al. A genetic signature of interspecies variations in gene expression. Nat Genet 38, 830–834 (2006). https://doi.org/10.1038/ng1819

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