Home LiteratureArticle Details
PMID: 20231876 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Evolutionary tinkering with conserved components of a transcriptional regulatory network.

PLoS biology ·Vol. 8 ·No. 3 ·2010-03-09 ·Pages e1000329

Lavoie H, Hogues H, Mallick J, Sellam A, Nantel A, Whiteway M

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.

MeSH Terms
Base Sequence Biological Evolution Candida albicans/genetics,metabolism DNA, Fungal/genetics,metabolism Fungal Proteins/genetics,metabolism Gene Expression Regulation, Fungal Gene Regulatory Networks Genome, Fungal Microarray Analysis Molecular Sequence Data Regulon Ribosomes/genetics,metabolism Saccharomyces cerevisiae/genetics,metabolism Signal Transduction/physiology Transcription Factors/genetics,metabolism
Chemicals
DNA, Fungal Fungal Proteins Transcription Factors
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Lavoie Hugo
Biotechnology Research Institute, National Research Council, Montreal, Quebec, Canada.
Hogues Hervé
Mallick Jaideep
Sellam Adnane
Nantel André
Whiteway Malcolm
Conflict of Interest

The authors have declared that no competing interests exist.

References (119)
119 references, click to expand
  1. Microarray profiling of phage-display selections for rapid mapping of transcription factor-DNA interactions.
    PLoS Genet. 2009 Apr;5(4):e1000449 PMID: 19360118
  2. Rpd3p relocation mediates a transcriptional response to rapamycin in yeast.
    Chem Biol. 2004 Mar;11(3):295-9 PMID: 15123258
  3. Emerging principles of regulatory evolution.
    Proc Natl Acad Sci U S A. 2007 May 15;104 Suppl 1:8605-12 PMID: 17494759
  4. The protein kinase Tor1 regulates adhesin gene expression in Candida albicans.
    PLoS Pathog. 2009 Feb;5(2):e1000294 PMID: 19197361
  5. Network motifs: simple building blocks of complex networks.
    Science. 2002 Oct 25;298(5594):824-7 PMID: 12399590
  6. Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila.
    Nature. 2005 Feb 3;433(7025):481-7 PMID: 15690032
  7. Role of the N-terminal region of Rap1p in the transcriptional activation of glycolytic genes in Saccharomyces cerevisiae.
    Yeast. 2004 Jul 30;21(10):851-66 PMID: 15300680
  8. Transcriptional regulation of carbohydrate metabolism in the human pathogen Candida albicans.
    PLoS Pathog. 2009 Oct;5(10):e1000612 PMID: 19816560
  9. The evolutionary significance of cis-regulatory mutations.
    Nat Rev Genet. 2007 Mar;8(3):206-16 PMID: 17304246
  10. Evolution of chromosome organization driven by selection for reduced gene expression noise.
    Nat Genet. 2007 Aug;39(8):945-9 PMID: 17660811
  11. Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning.
    PLoS Biol. 2005 Dec;3(12):e384 PMID: 16248679
  12. A yeast hybrid provides insight into the evolution of gene expression regulation.
    Science. 2009 May 1;324(5927):659-62 PMID: 19407207
  13. Yeast two-hybrid vectors and strains.
    Methods Mol Biol. 2001;177:41-84 PMID: 11530616
  14. Genome-wide patterns of histone modifications in yeast.
    Nat Rev Mol Cell Biol. 2006 Sep;7(9):657-66 PMID: 16912715
  15. Pathogenic adaptation of intracellular bacteria by rewiring a cis-regulatory input function.
    Proc Natl Acad Sci U S A. 2009 Mar 10;106(10):3982-7 PMID: 19234126
  16. Regulatory changes underlying expression differences within and between Drosophila species.
    Nat Genet. 2008 Mar;40(3):346-50 PMID: 18278046
  17. TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1.
    Cell. 2004 Dec 29;119(7):969-79 PMID: 15620355
  18. Bifurcation analysis of the regulatory modules of the mammalian G1/S transition.
    Bioinformatics. 2004 Jul 10;20(10):1506-11 PMID: 15231543
  19. Evolution of the holozoan ribosome biogenesis regulon.
    BMC Genomics. 2008;9:442 PMID: 18816399
  20. Continuity in evolution: on the nature of transitions.
    Science. 1998 May 29;280(5368):1451-5 PMID: 9603737
  21. The evolution of hierarchical gene regulatory networks.
    Nat Rev Genet. 2009 Feb;10(2):141-8 PMID: 19139764
  22. The last common bilaterian ancestor.
    Development. 2002 Jul;129(13):3021-32 PMID: 12070079
  23. Impact of Transcription Units rearrangement on the evolution of the regulatory network of gamma-proteobacteria.
    BMC Genomics. 2008;9:128 PMID: 18366643
  24. A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size.
    Genes Dev. 2004 Oct 15;18(20):2491-505 PMID: 15466158
  25. Gene regulatory networks and the evolution of animal body plans.
    Science. 2006 Feb 10;311(5762):796-800 PMID: 16469913
  26. Bacterial regulatory networks are extremely flexible in evolution.
    Nucleic Acids Res. 2006;34(12):3434-45 PMID: 16840530
  27. Global analysis of protein expression in yeast.
    Nature. 2003 Oct 16;425(6959):737-41 PMID: 14562106
  28. A synthetic gene-metabolic oscillator.
    Nature. 2005 May 5;435(7038):118-22 PMID: 15875027
  29. Sfp1 is a stress- and nutrient-sensitive regulator of ribosomal protein gene expression.
    Proc Natl Acad Sci U S A. 2004 Oct 5;101(40):14315-22 PMID: 15353587
  30. The origin of protein interactions and allostery in colocalization.
    Nature. 2007 Dec 13;450(7172):983-90 PMID: 18075577
  31. Subtelomeric proteins negatively regulate telomere elongation in budding yeast.
    EMBO J. 2006 Feb 22;25(4):846-56 PMID: 16467854
  32. Genetics of global gene expression.
    Nat Rev Genet. 2006 Nov;7(11):862-72 PMID: 17047685
  33. Transcription factor substitution during the evolution of fungal ribosome regulation.
    Mol Cell. 2008 Mar 14;29(5):552-62 PMID: 18342603
  34. Phylogenetic motif detection by expectation-maximization on evolutionary mixtures.
    Pac Symp Biocomput. 2004;:324-35 PMID: 14992514
  35. GCR1, a transcriptional activator in Saccharomyces cerevisiae, complexes with RAP1 and can function without its DNA binding domain.
    EMBO J. 1993 Jun;12(6):2431-7 PMID: 8508768
  36. Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene.
    Nature. 2006 Apr 20;440(7087):1050-3 PMID: 16625197
  37. Neocentromeres form efficiently at multiple possible loci in Candida albicans.
    PLoS Genet. 2009 Mar;5(3):e1000400 PMID: 19266018
  38. Non-linear dynamics of cardiac excitation and impulse propagation.
    Nature. 1987 Dec 24-31;330(6150):749-52 PMID: 3696239
  39. Multiple sequence alignment with the Clustal series of programs.
    Nucleic Acids Res. 2003 Jul 1;31(13):3497-500 PMID: 12824352
  40. Orthologous transcription factors in bacteria have different functions and regulate different genes.
    PLoS Comput Biol. 2007 Sep;3(9):1739-50 PMID: 17845071
  41. Analysis of mammalian gene batteries reveals both stable ancestral cores and highly dynamic regulatory sequences.
    Genome Biol. 2008;9(12):R172 PMID: 19087242
  42. Actively transcribed rRNA genes in S. cerevisiae are organized in a specialized chromatin associated with the high-mobility group protein Hmo1 and are largely devoid of histone molecules.
    Genes Dev. 2008 May 1;22(9):1190-204 PMID: 18451108
  43. Bmp4 and morphological variation of beaks in Darwin's finches.
    Science. 2004 Sep 3;305(5689):1462-5 PMID: 15353802
  44. Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins.
    Genome Biol. 2006;7(3):R23 PMID: 16563186
  45. Genome evolution in yeasts.
    Nature. 2004 Jul 1;430(6995):35-44 PMID: 15229592
  46. Resurrecting the role of transcription factor change in developmental evolution.
    Evolution. 2008 Sep;62(9):2131-54 PMID: 18564379
  47. A toolbox for epitope-tagging and genome-wide location analysis in Candida albicans.
    BMC Genomics. 2008;9:578 PMID: 19055720
  48. Growth-regulated recruitment of the essential yeast ribosomal protein gene activator Ifh1.
    Nature. 2004 Dec 23;432(7020):1058-61 PMID: 15616569
  49. Transcriptional regulatory networks and the yeast cell cycle.
    Curr Opin Cell Biol. 2002 Dec;14(6):676-83 PMID: 12473339
  50. GO::TermFinder--open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes.
    Bioinformatics. 2004 Dec 12;20(18):3710-5 PMID: 15297299
  51. Reliable prediction of transcription factor binding sites by phylogenetic verification.
    Proc Natl Acad Sci U S A. 2005 Nov 22;102(47):16945-50 PMID: 16286651
  52. Transcriptional regulatory code of a eukaryotic genome.
    Nature. 2004 Sep 2;431(7004):99-104 PMID: 15343339
  53. The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches.
    Nature. 2006 Aug 3;442(7102):563-7 PMID: 16885984
  54. Frequent gain and loss of functional transcription factor binding sites.
    PLoS Comput Biol. 2007 May;3(5):e99 PMID: 17530920
  55. Comprehensive analysis of combinatorial regulation using the transcriptional regulatory network of yeast.
    J Mol Biol. 2006 Jun 30;360(1):213-27 PMID: 16762362
  56. Evolutionary dynamics of prokaryotic transcriptional regulatory networks.
    J Mol Biol. 2006 Apr 28;358(2):614-33 PMID: 16530225
  57. Evolution of transcriptional regulatory circuits in bacteria.
    Cell. 2009 Jul 23;138(2):233-44 PMID: 19632175
  58. RPD3 is required for the inactivation of yeast ribosomal DNA genes in stationary phase.
    EMBO J. 2002 Sep 16;21(18):4959-68 PMID: 12234935
  59. Evolutionary plasticity of polycomb/trithorax response elements in Drosophila species.
    PLoS Biol. 2008 Oct 28;6(10):e261 PMID: 18959483
  60. The tor pathway regulates gene expression by linking nutrient sensing to histone acetylation.
    Mol Cell Biol. 2003 Jan;23(2):629-35 PMID: 12509460
  61. The different (sur)faces of Rap1p.
    Mol Genet Genomics. 2003 Mar;268(6):791-8 PMID: 12655405
  62. Genetic interactions between transcription factors cause natural variation in yeast.
    Science. 2009 Jan 23;323(5913):498-501 PMID: 19164747
  63. Plasticity of telomere maintenance mechanisms in yeast.
    Trends Biochem Sci. 2010 Jan;35(1):8-17 PMID: 19846312
  64. Eukaryotic gene regulation in three dimensions and its impact on genome evolution.
    Curr Opin Genet Dev. 2008 Dec;18(6):571-82 PMID: 19007886
  65. Multifunctional centromere binding factor 1 is essential for chromosome segregation in the human pathogenic yeast Candida glabrata.
    Mol Cell Biol. 2001 Aug;21(15):4875-88 PMID: 11438645
  66. Sex determination across evolution: connecting the dots.
    PLoS Biol. 2005 Jan;3(1):e21 PMID: 15660158
  67. The transcription factor Ifh1 is a key regulator of yeast ribosomal protein genes.
    Nature. 2004 Dec 23;432(7020):1054-8 PMID: 15616568
  68. Rearrangements of the transcriptional regulatory networks of metabolic pathways in fungi.
    Curr Opin Microbiol. 2009 Dec;12(6):655-63 PMID: 19875326
  69. Comparative gene expression analysis by differential clustering approach: application to the Candida albicans transcription program.
    PLoS Genet. 2005 Sep;1(3):e39 PMID: 16470937
  70. RAP1 protein interacts with yeast telomeres in vivo: overproduction alters telomere structure and decreases chromosome stability.
    Cell. 1990 Nov 16;63(4):739-50 PMID: 2225074
  71. Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes.
    Dev Cell. 2006 Apr;10(4):531-8 PMID: 16580997
  72. Gene expression divergence in yeast is coupled to evolution of DNA-encoded nucleosome organization.
    Nat Genet. 2009 Apr;41(4):438-45 PMID: 19252487
  73. Bifurcation analysis of a model of the budding yeast cell cycle.
    Chaos. 2004 Sep;14(3):653-61 PMID: 15446975
  74. Fitting a mixture model by expectation maximization to discover motifs in biopolymers.
    Proc Int Conf Intell Syst Mol Biol. 1994;2:28-36 PMID: 7584402
  75. Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique.
    Proc Natl Acad Sci U S A. 2004 Aug 3;101(31):11374-9 PMID: 15272074
  76. A single Hox3 gene with composite bicoid and zerknullt expression characteristics in non-Cyclorrhaphan flies.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):274-9 PMID: 11773616
  77. Central role of Ifh1p-Fhl1p interaction in the synthesis of yeast ribosomal proteins.
    EMBO J. 2005 Feb 9;24(3):533-42 PMID: 15692568
  78. Evolution of eukaryotic transcription circuits.
    Science. 2008 Mar 28;319(5871):1797-9 PMID: 18369141
  79. The crystal structure of the DNA-binding domain of yeast RAP1 in complex with telomeric DNA.
    Cell. 1996 Apr 5;85(1):125-36 PMID: 8620531
  80. Assembly of regulatory factors on rRNA and ribosomal protein genes in Saccharomyces cerevisiae.
    Mol Cell Biol. 2007 Oct;27(19):6686-705 PMID: 17646381
  81. Genome-wide mapping of the coactivator Ada2p yields insight into the functional roles of SAGA/ADA complex in Candida albicans.
    Mol Biol Cell. 2009 May;20(9):2389-400 PMID: 19279142
  82. The evolution of combinatorial gene regulation in fungi.
    PLoS Biol. 2008 Feb;6(2):e38 PMID: 18303948
  83. Interaction of yeast kinetochore proteins with centromere-protein/transcription factor Cbf1.
    Proc Natl Acad Sci U S A. 2000 Nov 7;97(23):12583-8 PMID: 11070082
  84. Transcriptional regulatory networks in Saccharomyces cerevisiae.
    Science. 2002 Oct 25;298(5594):799-804 PMID: 12399584
  85. Evolution and development: anchors away!
    Curr Biol. 2007 Mar 6;17(5):R172-4 PMID: 17339017
  86. Ribosome biogenesis: giant steps for a giant problem.
    Cell. 2004 Dec 29;119(7):901-2 PMID: 15620347
  87. Parallel evolution of Pitx1 underlies pelvic reduction in Scottish threespine stickleback (Gasterosteus aculeatus).
    J Hered. 2007 Sep-Oct;98(6):581-6 PMID: 17693397
  88. YEASTRACT-DISCOVERER: new tools to improve the analysis of transcriptional regulatory associations in Saccharomyces cerevisiae.
    Nucleic Acids Res. 2008 Jan;36(Database issue):D132-6 PMID: 18032429
  89. Estimating the prevalence and regulatory potential of the telomere looping effect in yeast transcription regulation.
    Cell Cycle. 2006 Oct;5(20):2354-63 PMID: 17102608
  90. Global position and recruitment of HATs and HDACs in the yeast genome.
    Mol Cell. 2004 Oct 22;16(2):199-209 PMID: 15494307
  91. High-resolution DNA-binding specificity analysis of yeast transcription factors.
    Genome Res. 2009 Apr;19(4):556-66 PMID: 19158363
  92. How the multifunctional yeast Rap1p discriminates between DNA target sites: a crystallographic analysis.
    J Mol Biol. 2000 Nov 10;303(5):693-707 PMID: 11061969
  93. The evolution of gene regulation underlies a morphological difference between two Drosophila sister species.
    Cell. 2008 Mar 7;132(5):783-93 PMID: 18329365
  94. An HMG protein, Hmo1, associates with promoters of many ribosomal protein genes and throughout the rRNA gene locus in Saccharomyces cerevisiae.
    Mol Cell Biol. 2006 May;26(9):3672-9 PMID: 16612005
  95. Sfp1 plays a key role in yeast ribosome biogenesis.
    Eukaryot Cell. 2003 Oct;2(5):1061-8 PMID: 14555489
  96. Transcriptional rewiring of fungal galactose-metabolism circuitry.
    Curr Biol. 2007 Jun 19;17(12):1007-13 PMID: 17540568
  97. Combinatorial control of gene expression by the three yeast repressors Mig1, Mig2 and Mig3.
    BMC Genomics. 2008;9:601 PMID: 19087243
  98. Principles of transcriptional regulation and evolution of the metabolic system in E. coli.
    Genome Res. 2009 Jan;19(1):79-91 PMID: 18836036
  99. RAP, RAP, open up! New wrinkles for RAP1 in yeast.
    Trends Genet. 2000 Feb;16(2):51-3 PMID: 10652526
  100. Divergence of transcription factor binding sites across related yeast species.
    Science. 2007 Aug 10;317(5839):815-9 PMID: 17690298
  101. Rap1 in Candida albicans: an unusual structural organization and a critical function in suppressing telomere recombination.
    Mol Cell Biol. 2010 Mar;30(5):1254-68 PMID: 20008550
  102. Natural history and evolutionary principles of gene duplication in fungi.
    Nature. 2007 Sep 6;449(7158):54-61 PMID: 17805289
  103. Multiple domains of repressor activator protein 1 contribute to facilitated binding of glycolysis regulatory protein 1.
    Proc Natl Acad Sci U S A. 1998 Nov 24;95(24):14112-7 PMID: 9826662
  104. Large-scale essential gene identification in Candida albicans and applications to antifungal drug discovery.
    Mol Microbiol. 2003 Oct;50(1):167-81 PMID: 14507372
  105. Conservation and evolution of cis-regulatory systems in ascomycete fungi.
    PLoS Biol. 2004 Dec;2(12):e398 PMID: 15534694
  106. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks.
    Nature. 2004 Apr 15;428(6984):717-23 PMID: 15085123
  107. Large-scale turnover of functional transcription factor binding sites in Drosophila.
    PLoS Comput Biol. 2006 Oct;2(10):e130 PMID: 17040121
  108. Fine-structure analysis of ribosomal protein gene transcription.
    Mol Cell Biol. 2006 Jul;26(13):4853-62 PMID: 16782874
  109. Molecular architecture of the kinetochore-microtubule attachment site is conserved between point and regional centromeres.
    J Cell Biol. 2008 May 19;181(4):587-94 PMID: 18474626
  110. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution.
    Cell. 2008 Jul 11;134(1):25-36 PMID: 18614008
  111. fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis.
    PLoS Biol. 2005 Jan;3(1):e6 PMID: 15630478
  112. Rewiring of the yeast transcriptional network through the evolution of motif usage.
    Science. 2005 Aug 5;309(5736):938-40 PMID: 16081737
  113. Evolutionary changes in cis and trans gene regulation.
    Nature. 2004 Jul 1;430(6995):85-8 PMID: 15229602
  114. Evolution of a bacterial regulon controlling virulence and Mg(2+) homeostasis.
    PLoS Genet. 2009 Mar;5(3):e1000428 PMID: 19300486
  115. Only centromeres can supply the partition system required for ARS function in the yeast Yarrowia lipolytica.
    J Mol Biol. 2001 Jan 12;305(2):203-17 PMID: 11124900
  116. Conservation and evolvability in regulatory networks: the evolution of ribosomal regulation in yeast.
    Proc Natl Acad Sci U S A. 2005 May 17;102(20):7203-8 PMID: 15883364
  117. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny.
    Comput Appl Biosci. 1996 Dec;12(6):543-8 PMID: 9021275
  118. Transcriptional regulation constrains the organization of genes on eukaryotic chromosomes.
    Proc Natl Acad Sci U S A. 2008 Oct 14;105(41):15761-6 PMID: 18840678
  119. A conserved sequence motif within the exceptionally diverse telomeric sequences of budding yeasts.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3453-7 PMID: 8159768
Article Info
Journal
PLoS biology
Abbr.
PLoS Biol
ISSN
1545-7885
DOI
10.1371/journal.pbio.1000329
Published
2010-03-09
Epub
2010-00-09
Pages
e1000329
Language
English
Region
United States
NLM ID
101183755
PMCID
PMC2834713
Subset
IM
Grants
Canadian Institutes of Health Research · 42516-3 · Canada
Canadian Institutes of Health Research · MOP-84341 · Canada
External Links
PubMed source DOI: 10.1371/journal.pbio.1000329 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2