Evolutionary Tinkering with Conserved Components of a Transcriptional Regulatory Network

Overview

Journal PLoS Biol

Specialty Biology

Date 2010 Mar 17

PMID 20231876

Citations 92

Authors

Hugo Lavoie

Herve Hogues

Jaideep Mallick

Adnane Sellam

Andre Nantel

Malcolm Whiteway

Affiliations

Soon will be listed here.

Abstract

Gene expression variation between species is a major contributor to phenotypic diversity, yet the underlying flexibility of transcriptional regulatory networks remains largely unexplored. Transcription of the ribosomal regulon is a critical task for all cells; in S. cerevisiae the transcription factors Rap1, Fhl1, Ifh1, and Hmo1 form a multi-subunit complex that controls ribosomal gene expression, while in C. albicans this regulation is under the control of Tbf1 and Cbf1. Here, we analyzed, using full-genome transcription factor mapping, the roles, in both S. cerevisiae and C. albicans, of each orthologous component of this complete set of regulators. We observe dramatic changes in the binding profiles of the generalist regulators Cbf1, Hmo1, Rap1, and Tbf1, while the Fhl1-Ifh1 dimer is the only component involved in ribosomal regulation in both fungi: it activates ribosomal protein genes and rDNA expression in a Tbf1-dependent manner in C. albicans and a Rap1-dependent manner in S. cerevisiae. We show that the transcriptional regulatory network governing the ribosomal expression program of two related yeast species has been massively reshaped in cis and trans. Changes occurred in transcription factor wiring with cellular functions, movements in transcription factor hierarchies, DNA-binding specificity, and regulatory complexes assembly to promote global changes in the architecture of the fungal transcriptional regulatory network.

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References

Freckleton G, Lippman S, Broach J, Tavazoie S . Microarray profiling of phage-display selections for rapid mapping of transcription factor-DNA interactions. PLoS Genet. 2009; 5(4):e1000449. PMC: 2659770. DOI: 10.1371/journal.pgen.1000449. View

Humphrey E, Shamji A, Bernstein B, Schreiber S . Rpd3p relocation mediates a transcriptional response to rapamycin in yeast. Chem Biol. 2004; 11(3):295-9. DOI: 10.1016/j.chembiol.2004.03.001. View

Prudhomme B, Gompel N, Carroll S . Emerging principles of regulatory evolution. Proc Natl Acad Sci U S A. 2007; 104 Suppl 1:8605-12. PMC: 1876436. DOI: 10.1073/pnas.0700488104. View

Bastidas R, Heitman J, Cardenas M . The protein kinase Tor1 regulates adhesin gene expression in Candida albicans. PLoS Pathog. 2009; 5(2):e1000294. PMC: 2631134. DOI: 10.1371/journal.ppat.1000294. View

Milo R, Itzkovitz S, Kashtan N, Chklovskii D, Alon U . Network motifs: simple building blocks of complex networks. Science. 2002; 298(5594):824-7. DOI: 10.1126/science.298.5594.824. View

Gompel N, Prudhomme B, Wittkopp P, Kassner V, Carroll S . Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature. 2005; 433(7025):481-7. DOI: 10.1038/nature03235. View

Mizuno T, Kishimoto T, Shinzato T, Haw R, Chambers A, Wood J . Role of the N-terminal region of Rap1p in the transcriptional activation of glycolytic genes in Saccharomyces cerevisiae. Yeast. 2004; 21(10):851-66. DOI: 10.1002/yea.1123. View

Askew C, Sellam A, Epp E, Hogues H, Mullick A, Nantel A . Transcriptional regulation of carbohydrate metabolism in the human pathogen Candida albicans. PLoS Pathog. 2009; 5(10):e1000612. PMC: 2749448. DOI: 10.1371/journal.ppat.1000612. View

Wray G . The evolutionary significance of cis-regulatory mutations. Nat Rev Genet. 2007; 8(3):206-16. DOI: 10.1038/nrg2063. View

10.

Batada N, Hurst L . Evolution of chromosome organization driven by selection for reduced gene expression noise. Nat Genet. 2007; 39(8):945-9. DOI: 10.1038/ng2071. View

11.

Guillemette B, Bataille A, Gevry N, Adam M, Blanchette M, Robert F . Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol. 2005; 3(12):e384. PMC: 1275524. DOI: 10.1371/journal.pbio.0030384. View

12.

Tirosh I, Reikhav S, Levy A, Barkai N . A yeast hybrid provides insight into the evolution of gene expression regulation. Science. 2009; 324(5927):659-62. DOI: 10.1126/science.1169766. View

13.

James P . Yeast two-hybrid vectors and strains. Methods Mol Biol. 2001; 177:41-84. DOI: 10.1385/1-59259-210-4:041. View

14.

Millar C, Grunstein M . Genome-wide patterns of histone modifications in yeast. Nat Rev Mol Cell Biol. 2006; 7(9):657-66. DOI: 10.1038/nrm1986. View

15.

Osborne S, Walthers D, Tomljenovic A, Mulder D, Silphaduang U, Duong N . Pathogenic adaptation of intracellular bacteria by rewiring a cis-regulatory input function. Proc Natl Acad Sci U S A. 2009; 106(10):3982-7. PMC: 2645909. DOI: 10.1073/pnas.0811669106. View

16.

Wittkopp P, Haerum B, Clark A . Regulatory changes underlying expression differences within and between Drosophila species. Nat Genet. 2008; 40(3):346-50. DOI: 10.1038/ng.77. View

17.

Martin D, Soulard A, Hall M . TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell. 2004; 119(7):969-79. DOI: 10.1016/j.cell.2004.11.047. View

18.

Swat M, Kel A, Herzel H . Bifurcation analysis of the regulatory modules of the mammalian G1/S transition. Bioinformatics. 2004; 20(10):1506-11. DOI: 10.1093/bioinformatics/bth110. View

19.

Brown S, Cole M, Erives A . Evolution of the holozoan ribosome biogenesis regulon. BMC Genomics. 2008; 9:442. PMC: 2570694. DOI: 10.1186/1471-2164-9-442. View

20.

Fontana W, Schuster P . Continuity in evolution: on the nature of transitions. Science. 1998; 280(5368):1451-5. DOI: 10.1126/science.280.5368.1451. View