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

Significance Independent transitions to multicellularity in eukaryotes involved the evolution of complex transcriptional regulation toolkits to control cell differentiation. By using comparative genomics, we show that plants and animals required richer transcriptional machineries compared with other eukaryotic multicellular lineages. We suggest this is due to their orchestrated embryonic development. Moreover, our analysis of transcription factor (TF) expression patterns during the development of animals reveal links between TF evolution, species ontogeny, and the phylotypic stage. 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.

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