Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages

Proc Natl Acad Sci U S A. 2013 Dec 10;110(50):E4858-66. doi: 10.1073/pnas.1311818110. Epub 2013 Nov 25.

Abstract

Transcription factors (TFs) are the main players in transcriptional regulation in eukaryotes. However, it remains unclear what role TFs played in the origin of all of the different eukaryotic multicellular lineages. In this paper, we explore how the origin of TF repertoires shaped eukaryotic evolution and, in particular, their role into the emergence of multicellular lineages. We traced the origin and expansion of all known TFs through the eukaryotic tree of life, using the broadest possible taxon sampling and an updated phylogenetic background. Our results show that the most complex multicellular lineages (i.e., those with embryonic development, Metazoa and Embryophyta) have the most complex TF repertoires, and that these repertoires were assembled in a stepwise manner. We also show that a significant part of the metazoan and embryophyte TF toolkits evolved earlier, in their respective unicellular ancestors. To gain insights into the role of TFs in the development of both embryophytes and metazoans, we analyzed TF expression patterns throughout their ontogeny. The expression patterns observed in both groups recapitulate those of the whole transcriptome, but reveal some important differences. Our comparative genomics and expression data reshape our view on how TFs contributed to eukaryotic evolution and reveal the importance of TFs to the origins of multicellularity and embryonic development.

Keywords: Holozoa; LECA; phylotypic stage.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Differentiation / genetics*
  • Computational Biology
  • Embryonic Development / genetics*
  • Eukaryota / genetics*
  • Evolution, Molecular*
  • Gene Expression Regulation, Developmental / genetics*
  • Genomics / methods
  • Statistics, Nonparametric
  • Transcription Factors / genetics*

Substances

  • Transcription Factors

Associated data

  • SRA/SRX096925
  • SRA/SRX096927
  • SRA/SRX377507
  • SRA/SRX377508
  • SRA/SRX377514