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Nucleic Acids Research Advance Access published online on April 16, 2009
Nucleic Acids Research, doi:10.1093/nar/gkp231
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© 2009 The Author(s)
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Gene Regulation, Chromatin, and Epigenetics

Transcriptional regulation shapes the organization of genes on bacterial chromosomes

Sarath Chandra Janga1,*, Heladia Salgado2 and Agustino Martínez-Antonio3,*

1MRC Laboratory of Molecular Biology, Hills Road, Cambridge CB2 0QH, UK, 2Programa de Genómica Computacional. Centro de Ciencias Genómicas. Universidad, Nacional Autónoma de México. Cuernavaca, Morelos, 62100 and 3Departamento de Ingeniería Genética, Centro de Investigación y de Estudios Avanzados, Instituto Politécnico Nacional, Campus Guanajuato, Irapuato, 36500, México

*To whom correspondence should be addressed. Tel: +44 1223 402479; Fax: +44 1223 213556; Email: sarath{at}mrc-lmb.cam.ac.uk

Received January 25, 2009. Revised February 20, 2009. Accepted March 26, 2009.

Transcription factors (TFs) are the key elements responsible for controlling the expression of genes in bacterial genomes and when visualized on a genomic scale form a dense network of transcriptional interactions among themselves and with other protein coding genes. Although the structure of transcriptional regulatory networks (TRNs) is well understood, it is not clear what constrains govern them. Here, we explore this question using the TRNs of model prokaryotes and provide a link between the transcriptional hierarchy of regulons and their genome organization. We show that, to drive the kinetics and concentration gradients, TFs belonging to big and small regulons, depending on the number of genes they regulate, organize themselves differently on the genome with respect to their targets. We then propose a conceptual model that can explain how the hierarchical structure of TRNs might be ultimately governed by the dynamic biophysical requirements for targeting DNA-binding sites by TFs. Our results suggest that the main parameters defining the position of a TF in the network hierarchy are the number and chromosomal distances of the genes they regulate and their protein concentration gradients. These observations give insights into how the hierarchical structure of transcriptional networks can be encoded on the chromosome to drive the kinetics and concentration gradients of TFs depending on the number of genes they regulate and could be a common theme valid for other prokaryotes, proposing the role of transcriptional regulation in shaping the organization of genes on a chromosome.


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[Abstract] [Full Text] [PDF]


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