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

Abstract

Control over gene transcription is one of the main regulatory systems in eukaryotes. Transcription Factors (TFs) have a central role in this system, as they bind to DNA and enhance or inhibit gene expression. Although previous studies analysed the evolutionary history of TFs, it remains unclear what role TFs played in the origin of all 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 with embryonic development, Metazoa and Embryophyta) have the most complex TF repertoires, and that these repertoires were assembled in a step-wise manner. We also show that a significant part of the metazoan and embryophyte TF toolkits evolved much earlier, in their respective unicellular ancestors. To gain insights into the role of TFs in the development of both embryophytes and metazoans, we analysed TF expression patterns throughout their ontogeny. The expression patterns observed in both groups recapitulate those of the whole transcriptome, but reveal important differences. In particular, gastrulation in animals is defined by metazoan-specific TFs, while later development in embryophytes is characterised by an enrichment in archaeplastid-specific TFs. We suggest that these differences are due to the difference between the closed and open development of extant metazoans and embryophytes, respectively. Our comparative genomics and expression data re-shapes our view on how TFs contributed to eukaryotic evolution and reveals the importance of TFs to the origins of multicellularity and embryonic development.