Parallel Evolution of Transcription Factors in Basal Metazoans

Abstract

Transcription factors (TFs) play a pivotal role as regulators of gene expression, orchestrating the formation and maintenance of diverse animal body plans and innovations. However, the precise contributions of TFs and the underlying mechanisms driving the origin of basal metazoan body plans, particularly in ctenophores, remain elusive. Here, we present a comprehensive catalog of TFs in 2 ctenophore species, Pleurobrachia bachei and Mnemiopsis leidyi, revealing 428 and 418 TFs in their respective genomes. In contrast, morphologically simpler metazoans have a reduced TF representation compared to ctenophores, cnidarians, and bilaterians: the sponge Amphimedon encodes 277 TFs, and the placozoan Trichoplax adhaerens encodes 274 TFs. The emergence of complex ctenophore tissues and organs coincides with significant lineage-specific diversification of the zinc finger C2H2 (ZF-C2H2) and homeobox superfamilies of TFs. Notable, the lineages leading to Amphimedon and Trichoplax exhibit independent expansions of leucine zipper (BZIP) TFs. Some lineage-specific TFs may have evolved through the domestication of mobile elements, thereby supporting alternative mechanisms of parallel TF evolution and body plan diversification across the Metazoa.

Keywords: Amphimedon; BHLH; Ctenophora; Evolution of animal complexity; Genome; Homeobox; Mnemiopsis; Neurons; Placozoa; Pleurobrachia; Porifera; Transcription factors; Transposons; Trichoplax.