Insights into deuterostome evolution from the biphasic transcriptional programmes of hemichordates

Evolutionary history of deuterostomes remains unsolved and is intimately related to the origin of chordates. Among deuterostomes, hemichordates and echinoderms (collectively called Ambulacraria) are sister groups of chordates. Comparative studies involving these three groups provide valuable insights into deuterostome evolution. Indirect developing hemichordates produce planktonic larvae that bear resemblance to echinoderm larvae before undergoing metamorphosis into an adult body plan with anteroposterior polarity homologous to that of chordates. Therefore, understanding the developmental processes of indirect-developing hemichordates can help understand the evolution of deuterostomes and the origins of chordates. In this study, we analysed the transcriptomes and chromatin accessibility of multiple developmental stages of the indirect-developing hemichordate Ptychodera flava and discovered that it exhibits a biphasic developmental program controlled by distinct sets of transcription factors and their corresponding regulatory elements. Comparative analyses of transcriptomes and network analyses revealed that the gastrula transcriptome is relatively ancient, and the TFs orchestrating its gene expression are highly interconnected in networks of cis-regulatory interactions. Comparing the developmental transcriptomes of hemichordates, echinoderms, and amphioxus, revealed high conservation of gene expression during gastrulation that extends to the neurula stages of amphioxus, along with remarkable similarity in larval transcriptomes across the three species. Additionally, we show that P. flava possesses conserved interactions of transcription factors necessary for the development of echinoderm endomesoderm and chordate axial mesoderm, including conserved cis-regulatory elements of the FoxA transcription factor that is central to the two networks. These findings suggest the existence of a deuterostome phylotypic stage during gastrulation governed by gene regulatory networks with conserved cis-regulatory interactions. Conversely, integration of gene expression data with synteny data revealed that gene expression recapitulates the independent evolutionary history of the Ancestral Linkage Groups that underwent rearrangements in each deuterostome lineage, suggesting a potential role of genome rearrangement during the evolution of larval strategies in hemichordates and deuterostome body plans.