Transcription factor evolution and the origins of multicellulariyy in eukaryotic lineages

Abstract

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

We have analyzed the Transcription Factor repertoire for 71 eukaryotic genomes, and we have traced the evolutionary histories, diversification, architectural reconfiguration and ancestral composition across the eukaryotic tree of life. Moreover we have analyzed developmental expression datasets for TF activity in model species such as Danio rerio, Drosophila melanogaster, Arabidopsis thaliana.

Our results show that the most complex multicellular lineages (i.e., those with with em- bryonic 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 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. We suggest that these diffe- rences are due to the difference between the determined and indetermined develop- ment 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 deve- lopment.