Rewiring of the Yeast Transcriptional Network Through the Evolution of Motif Usage

Recent experiments revealed large-scale differences in the transcription programs of related species, yet little is known about the genetic basis underlying the evolution of gene expression and its contribution to phenotypic diversity. Here we describe a large-scale modulation of the yeast transcription program that is connected to the emergence of the capacity for rapid anaerobic growth. Genes coding for mitochondrial and cytoplasmic ribosomal proteins display a strongly correlated expression pattern in Candida albicans, but this correlation is lost in the fermentative yeast Saccharomyces cerevisiae. We provide evidence that this change in gene expression is connected to the loss of a specific cis-regulatory element from dozens of genes following the apparent whole-genome duplication event. Our results shed new light on the genetic mechanisms underlying the large-scale evolution of transcriptional networks.

[1]  K. H. Wolfe,et al.  Molecular evidence for an ancient duplication of the entire yeast genome , 1997, Nature.

[2]  K. Wolfe.  Evolutionary Genomics: Yeasts Accelerate beyond BLAST , 2004, Current Biology.

[3]  P. Philippsen,et al.  The Ashbya gossypii Genome as a Tool for Mapping the Ancient Saccharomyces cerevisiae Genome , 2004, Science.

[4]  George M. Church,et al.  Quantitative whole-genome analysis of DNA-protein interactions by in vivo methylase protection in E. coli , 1998, Nature Biotechnology.

[5]  A. Regev,et al.  Conservation and evolvability in regulatory networks: the evolution of ribosomal regulation in yeast. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[6]  M. King,et al.  Evolution at two levels in humans and chimpanzees. , 1975, Science.

[7]  S. Bergmann,et al.  Similarities and Differences in Genome-Wide Expression Data of Six Organisms , 2003, PLoS biology.

[8]  S. Carroll.  Endless Forms The Evolution of Gene Regulation and Morphological Diversity , 2000, Cell.

[9]  E. Davidson.  Genomic Regulatory Systems: Development and Evolution , 2005 .

[10]  Yaniv Ziv,et al.  Revealing modular organization in the yeast transcriptional network , 2002, Nature Genetics.

[11]  Alan M. Moses,et al.  Conservation and Evolution of Cis-Regulatory Systems in Ascomycete Fungi , 2004, PLoS biology.

[12]  A. Kimura,et al.  Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing , 2002, Nature Genetics.

[13]  J. Piškur,et al.  Yeast genome sequencing: the power of comparative genomics , 2004, Molecular microbiology.

[14]  B. Birren,et al.  Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae , 2004, Nature.

[15]  Hans-Joachim Schüller,et al.  Transcriptional control of nonfermentative metabolism in the yeast Saccharomyces cerevisiae , 2003, Current Genetics.