Heterochronic evolution reveals modular timing changes in budding yeast transcriptomes.
BACKGROUND
Gene expression is a dynamic trait, and the evolution of gene regulation can dramatically alter the timing of gene expression without greatly affecting mean expression levels. Moreover, modules of co-regulated genes may exhibit coordinated shifts in expression timing patterns during evolutionary divergence. Here, we examined transcriptome evolution in the dynamical context of the budding yeast cell-division cycle, to investigate the extent of divergence in expression timing and the regulatory architecture underlying timing evolution.


RESULTS
Using a custom microarray platform, we obtained 378 measurements for 6,263 genes over 18 timepoints of the cell-division cycle in nine strains of S. cerevisiae and one strain of S. paradoxus. Most genes show significant divergence in expression dynamics at all scales of transcriptome organization, suggesting broad potential for timing changes. A model test comparing expression level evolution versus timing evolution revealed a better fit with timing evolution for 82% of genes. Analysis of shared patterns of timing evolution suggests the existence of seven dynamically-autonomous modules, each of which shows coherent evolutionary timing changes. Analysis of transcription factors associated with these gene modules suggests a modular pleiotropic source of divergence in expression timing.


CONCLUSIONS
We propose that transcriptome evolution may generally entail changes in timing (heterochrony) rather than changes in levels (heterometry) of expression. Evolution of gene expression dynamics may involve modular changes in timing control mediated by module-specific transcription factors. We hypothesize that genome-wide gene regulation may utilize a general architecture comprised of multiple semi-autonomous event timelines, whose superposition could produce combinatorial complexity in timing control patterns.
Simola
Daniel F
DF
Department of Biology, University of Pennsylvania, 433 S, University Ave, Philadelphia, PA 19104, USA. simola@mail.med.upenn.edu
Francis
Chantal
C
Sniegowski
Paul D
PD
Kim
Junhyong
J
D002453:Cell Cycle; D019143:Evolution, Molecular; D020869:Gene Expression Profiling; D015966:Gene Expression Regulation, Fungal; D053263:Gene Regulatory Networks; D014644:Genetic Variation; D020411:Oligonucleotide Array Sequence Analysis; D012331:RNA, Fungal / Q000235:genetics; D012441:Saccharomyces cerevisiae / Q000235:genetics*; D014157:Transcription Factors / Q000235:genetics
D012331:RNA, Fungal; D014157:Transcription Factors