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Gene duplication and co-evolution of G1/S transcription factor specificity in fungi are essential for optimizing cell fitness

Hendler, A; Medina, EM; Kishkevich, A; Abu-Qarn, M; Klier, S; Buchler, NE; de Bruin, RAM; (2017) Gene duplication and co-evolution of G1/S transcription factor specificity in fungi are essential for optimizing cell fitness. PLoS Genetics , 13 (5) , Article e1006778. 10.1371/journal.pgen.1006778. Green open access

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Abstract

Transcriptional regulatory networks play a central role in optimizing cell survival. How DNA binding domains and cis-regulatory DNA binding sequences have co-evolved to allow the expansion of transcriptional networks and how this contributes to cellular fitness remains unclear. Here we experimentally explore how the complex G1/S transcriptional network evolved in the budding yeast Saccharomyces cerevisiae by examining different chimeric transcription factor (TF) complexes. Over 200 G1/S genes are regulated by either one of the two TF complexes, SBF and MBF, which bind to specific DNA binding sequences, SCB and MCB, respectively. The difference in size and complexity of the G1/S transcriptional network across yeast species makes it well suited to investigate how TF paralogs (SBF and MBF) and DNA binding sequences (SCB and MCB) co-evolved after gene duplication to rewire and expand the network of G1/S target genes. Our data suggests that whilst SBF is the likely ancestral regulatory complex, the ancestral DNA binding element is more MCB-like. G1/S network expansion took place by both cis- and trans- co-evolutionary changes in closely related but distinct regulatory sequences. Replacement of the endogenous SBF DNA-binding domain (DBD) with that from more distantly related fungi leads to a contraction of the SBF-regulated G1/S network in budding yeast, which also correlates with increased defects in cell growth, cell size, and proliferation.

Type: Article
Title: Gene duplication and co-evolution of G1/S transcription factor specificity in fungi are essential for optimizing cell fitness
Open access status: An open access version is available from UCL Discovery
DOI: 10.1371/journal.pgen.1006778
Publisher version: https://doi.org/10.1371/journal.pgen.1006778
Language: English
Additional information: Copyright: © 2017 Hendler et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Lab for Molecular Cell Bio MRC-UCL
URI: https://discovery-pp.ucl.ac.uk/id/eprint/1562619
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