Hemichordate cis-regulatory genomics and the gene expression dynamics of deuterostomes

Abstract

Deuterostomes are one major group of bilaterians composed by hemichordates and echinoderms (collectively called Ambulacraria) and chordates. Comparative studies between these groups can provide valuable insights into the nature of the last common ancestor of deuterostomes and that of bilaterians. Indirect development of hemichordates, with larval phases similar to echinoderms and an adult body plan with an anteroposterior polarity like chordates and other bilaterians, makes them a suitable model for studying the molecular basis of development among deuterostomes. However, a comprehensive, quantitative catalogue of gene expression and chromatin dynamics in hemichordates is still lacking. In this study, we analysed the transcriptomes and chromatin accessibility of multiple developmental stages of the indirect-developing hemichordate Ptychodera flava. We observed that P. flava development is underpinned by a biphasic transcriptional program probably controlled by distinct genetic networks. Comparisons with other bilaterian species revealed similar transcriptional and regulatory dynamics during hemichordate gastrulation, cephalochordate neurulation and elongation stages of annelids. By means of regulatory networks analysis and functional validations by transgenesis experiments in echinoderms, we propose that gastrulation is the stage of highest molecular resemblance in deuterostomes and that much of the molecular basis of deuterostome development was probably present in the bilaterian last common ancestor. Analysis of transcriptomes and chromatin accessibility of multiple developmental stages of the indirect-developing hemichordate Ptychodera flava shows similar transcriptional dynamics of different developmental stages across hemichordates, echinoderms and chordates.