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Transcriptional regulatory code of a eukaryotic genome

Author

Listed:
  • Christopher T. Harbison

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center
    Massachusetts Institute of Technology)

  • D. Benjamin Gordon

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center)

  • Tong Ihn Lee

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center)

  • Nicola J. Rinaldi

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center
    Massachusetts Institute of Technology)

  • Kenzie D. Macisaac

    (MIT Computer Science and Artificial Intelligence Laboratory)

  • Timothy W. Danford

    (MIT Computer Science and Artificial Intelligence Laboratory)

  • Nancy M. Hannett

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center)

  • Jean-Bosco Tagne

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center)

  • David B. Reynolds

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center)

  • Jane Yoo

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center)

  • Ezra G. Jennings

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center)

  • Julia Zeitlinger

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center)

  • Dmitry K. Pokholok

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center)

  • Manolis Kellis

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center
    MIT Computer Science and Artificial Intelligence Laboratory
    Broad Institute)

  • P. Alex Rolfe

    (MIT Computer Science and Artificial Intelligence Laboratory)

  • Ken T. Takusagawa

    (MIT Computer Science and Artificial Intelligence Laboratory)

  • Eric S. Lander

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center
    Massachusetts Institute of Technology
    Broad Institute)

  • David K. Gifford

    (MIT Computer Science and Artificial Intelligence Laboratory
    Broad Institute)

  • Ernest Fraenkel

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center
    MIT Computer Science and Artificial Intelligence Laboratory)

  • Richard A. Young

    (Whitehead Institute for Biomedical Research, Nine Cambridge Center
    Massachusetts Institute of Technology
    Broad Institute)

Abstract

DNA-binding transcriptional regulators interpret the genome's regulatory code by binding to specific sequences to induce or repress gene expression1. Comparative genomics has recently been used to identify potential cis-regulatory sequences within the yeast genome on the basis of phylogenetic conservation2,3,4,5,6, but this information alone does not reveal if or when transcriptional regulators occupy these binding sites. We have constructed an initial map of yeast's transcriptional regulatory code by identifying the sequence elements that are bound by regulators under various conditions and that are conserved among Saccharomyces species. The organization of regulatory elements in promoters and the environment-dependent use of these elements by regulators are discussed. We find that environment-specific use of regulatory elements predicts mechanistic models for the function of a large population of yeast's transcriptional regulators.

Suggested Citation

  • Christopher T. Harbison & D. Benjamin Gordon & Tong Ihn Lee & Nicola J. Rinaldi & Kenzie D. Macisaac & Timothy W. Danford & Nancy M. Hannett & Jean-Bosco Tagne & David B. Reynolds & Jane Yoo & Ezra G., 2004. "Transcriptional regulatory code of a eukaryotic genome," Nature, Nature, vol. 431(7004), pages 99-104, September.
    • Handle: RePEc:nat:nature:v:431:y:2004:i:7004:d:10.1038_nature02800
    DOI: 10.1038/nature02800
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    Citations

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    Cited by:

    1. Harri Lähdesmäki & Alistair G Rust & Ilya Shmulevich, 2008. "Probabilistic Inference of Transcription Factor Binding from Multiple Data Sources," PLOS ONE, Public Library of Science, vol. 3(3), pages 1-24, March.
    2. Yue Yuan & Qiang Huo & Ziru Zhang & Qun Wang & Juanxia Wang & Shuaikang Chang & Peng Cai & Karen M. Song & David W. Galbraith & Weixiao Zhang & Long Huang & Rentao Song & Zeyang Ma, 2024. "Decoding the gene regulatory network of endosperm differentiation in maize," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. Jens Keilwagen & Jan Grau & Ivan A Paponov & Stefan Posch & Marc Strickert & Ivo Grosse, 2011. "De-Novo Discovery of Differentially Abundant Transcription Factor Binding Sites Including Their Positional Preference," PLOS Computational Biology, Public Library of Science, vol. 7(2), pages 1-13, February.
    4. Dana S F Homsi & Vineet Gupta & Gary D Stormo, 2009. "Modeling the Quantitative Specificity of DNA-Binding Proteins from Example Binding Sites," PLOS ONE, Public Library of Science, vol. 4(8), pages 1-9, August.
    5. Guo-Cheng Yuan & Jun S Liu, 2008. "Genomic Sequence Is Highly Predictive of Local Nucleosome Depletion," PLOS Computational Biology, Public Library of Science, vol. 4(1), pages 1-11, January.
    6. Anshul Kundaje & Xiantong Xin & Changgui Lan & Steve Lianoglou & Mei Zhou & Li Zhang & Christina Leslie, 2008. "A Predictive Model of the Oxygen and Heme Regulatory Network in Yeast," PLOS Computational Biology, Public Library of Science, vol. 4(11), pages 1-21, November.
    7. Armita Nourmohammad & Michael Lässig, 2011. "Formation of Regulatory Modules by Local Sequence Duplication," PLOS Computational Biology, Public Library of Science, vol. 7(10), pages 1-12, October.
    8. Manikandan Narayanan & Adrian Vetta & Eric E Schadt & Jun Zhu, 2010. "Simultaneous Clustering of Multiple Gene Expression and Physical Interaction Datasets," PLOS Computational Biology, Public Library of Science, vol. 6(4), pages 1-13, April.
    9. Kyoung-Jae Won & Saurabh Agarwal & Li Shen & Robert Shoemaker & Bing Ren & Wei Wang, 2009. "An Integrated Approach to Identifying Cis-Regulatory Modules in the Human Genome," PLOS ONE, Public Library of Science, vol. 4(5), pages 1-8, May.
    10. Saket Navlakha & Anthony Gitter & Ziv Bar-Joseph, 2012. "A Network-based Approach for Predicting Missing Pathway Interactions," PLOS Computational Biology, Public Library of Science, vol. 8(8), pages 1-13, August.
    11. Zing Tsung-Yeh Tsai & Shin-Han Shiu & Huai-Kuang Tsai, 2015. "Contribution of Sequence Motif, Chromatin State, and DNA Structure Features to Predictive Models of Transcription Factor Binding in Yeast," PLOS Computational Biology, Public Library of Science, vol. 11(8), pages 1-22, August.
    12. Sourav Bandyopadhyay & Ryan Kelley & Nevan J Krogan & Trey Ideker, 2008. "Functional Maps of Protein Complexes from Quantitative Genetic Interaction Data," PLOS Computational Biology, Public Library of Science, vol. 4(4), pages 1-8, April.
    13. Leelavati Narlikar & Raluca Gordân & Alexander J Hartemink, 2007. "A Nucleosome-Guided Map of Transcription Factor Binding Sites in Yeast," PLOS Computational Biology, Public Library of Science, vol. 3(11), pages 1-10, November.
    14. Jeremiah J Faith & Boris Hayete & Joshua T Thaden & Ilaria Mogno & Jamey Wierzbowski & Guillaume Cottarel & Simon Kasif & James J Collins & Timothy S Gardner, 2007. "Large-Scale Mapping and Validation of Escherichia coli Transcriptional Regulation from a Compendium of Expression Profiles," PLOS Biology, Public Library of Science, vol. 5(1), pages 1-13, January.
    15. Gross, Eitan, 2015. "Effect of environmental stress on regulation of gene expression in the yeast," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 430(C), pages 224-235.
    16. Joshua S Weitz & Philip N Benfey & Ned S Wingreen, 2007. "Evolution, Interactions, and Biological Networks," PLOS Biology, Public Library of Science, vol. 5(1), pages 1-3, January.
    17. Wei-Sheng Wu & Fu-Jou Lai, 2016. "Detecting Cooperativity between Transcription Factors Based on Functional Coherence and Similarity of Their Target Gene Sets," PLOS ONE, Public Library of Science, vol. 11(9), pages 1-12, September.
    18. Eilon Sharon & Shai Lubliner & Eran Segal, 2008. "A Feature-Based Approach to Modeling Protein–DNA Interactions," PLOS Computational Biology, Public Library of Science, vol. 4(8), pages 1-17, August.
    19. Rahul Siddharthan & Eric D Siggia & Erik van Nimwegen, 2005. "PhyloGibbs: A Gibbs Sampling Motif Finder That Incorporates Phylogeny," PLOS Computational Biology, Public Library of Science, vol. 1(7), pages 1-23, December.
    20. Xiaoyu Tu & Sibo Ren & Wei Shen & Jianjian Li & Yuxiang Li & Chuanshun Li & Yangmeihui Li & Zhanxiang Zong & Weibo Xie & Donald Grierson & Zhangjun Fei & Jim Giovannoni & Pinghua Li & Silin Zhong, 2022. "Limited conservation in cross-species comparison of GLK transcription factor binding suggested wide-spread cistrome divergence," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    21. Phaedra Agius & Aaron Arvey & William Chang & William Stafford Noble & Christina Leslie, 2010. "High Resolution Models of Transcription Factor-DNA Affinities Improve In Vitro and In Vivo Binding Predictions," PLOS Computational Biology, Public Library of Science, vol. 6(9), pages 1-12, September.
    22. Xiaoke Ma & Long Gao & Georgios Karamanlidis & Peng Gao & Chi Fung Lee & Lorena Garcia-Menendez & Rong Tian & Kai Tan, 2015. "Revealing Pathway Dynamics in Heart Diseases by Analyzing Multiple Differential Networks," PLOS Computational Biology, Public Library of Science, vol. 11(6), pages 1-19, June.
    23. Shojaie Ali & Michailidis George, 2010. "Network Enrichment Analysis in Complex Experiments," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 9(1), pages 1-36, May.
    24. Timothy E Reddy & Charles DeLisi & Boris E Shakhnovich, 2007. "Binding Site Graphs: A New Graph Theoretical Framework for Prediction of Transcription Factor Binding Sites," PLOS Computational Biology, Public Library of Science, vol. 3(5), pages 1-11, May.
    25. Kenzie D MacIsaac & Ernest Fraenkel, 2006. "Practical Strategies for Discovering Regulatory DNA Sequence Motifs," PLOS Computational Biology, Public Library of Science, vol. 2(4), pages 1-10, April.

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