Insights into deuterostome evolution from the biphasic transcriptional programme of hemichordates

Abstract

Evolutionary history of deuterostomes has remained unsolved and is intimately related to how chordates originated. Within the clade of deuterostomes, hemichordates and echinoderms (together called Ambulacraria) are sister groups of chordates; comparative studies among the three are insightful for understanding deuterostome evolution. Indirect-developing hemichordates, such as Ptychodera flava, develop into planktonic larvae, which are morphologically similar to echinoderm larvae, before metamorphosing into the adult body plan that retains an anteroposterior polarity homologous to that of chordates. Therefore, deciphering developmental programmes of indirect-developing hemichordates may provide a key for understanding the evolution of deuterostomes and chordate origins. Here, we characterise transcriptomes and chromatin accessibility across multiple developmental stages of P. flava and uncover biphasic developmental programmes controlled by different sets of transcription factors and their corresponding cis-regulatory elements. Transcriptome age and network analyses reveal that the gastrula transcriptome is relatively ancient and highly connected. By comparing developmental transcriptomes of hemichordate, sea urchin and amphioxus, a high conservation of gene expression during gastrulation is identified and extended to neurula stages of amphioxus, in addition to the highly similar larval transcriptomes among the three species. Moreover, P. flava possesses conserved interactions of transcription factors required for the development of echinoderm endomesoderm and chordate axial mesoderm. These results suggest a deuterostome phylotypic stage during gastrulation (corresponding to amphioxus gastrulation and neurulation) controlled by gene regulatory networks with conserved cis-regulatory interactions, and support the hypothesis that the deuterostome ancestor is an indirect-developer.

Chromosome-level genome assemblies of 2 hemichordates provide new insights into deuterostome origin and chromosome evolution

“…Taken together, our GO enrichment analyses provide a global view of possible regulatory and functional changes related to the lineage-specific chromosomal rearrangements. Such rearrangement events are in agreement with levels of divergence in gene expression profiles [42], supporting the hypothesis that at least some of these potential changes are plausibly associated with the evolution of distinct lineage-specific features and diverse body plans in deuterostomes.…”

“…Assembly of the 3 microsyntenic blocks into the deuterostome pharyngeal gene cluster plausibly contributes to the co-regulation of the genes. Indeed, similar temporal expression profiles of the pharyngeal cluster genes are observed among deuterostomes, while orthologs of these genes in protostome and non-bilaterian species display more divergent expression profiles [ 42 ]. These results support the idea that clustering of the pharyngeal genes in deuterostomes likely contributes to their co-regulation.…”

“…Second, the protein sequences from other species, including mouse, chick, zebrafish, spotted gar, sea lamprey, amphioxus, ascidian, sea urchin, and sea anemone, were aligned to the PFL genome assembly using GeMoMa (version 1.7) [ 61 ]. Third, the Illumina RNA-seq short reads from PFL at 16 stages [ 42 ] were mapped using STAR aligner (version 2.7.6a) [ 62 ]. The subsequent genome-guided transcript reconstruction was conducted with StringTie (version 2.1.4) [ 63 ] and CLASS2 (version 2.1.7) [ 64 ].…”

Chromosome-level genome assemblies of two hemichordates provide new insights into deuterostome origin and chromosome evolution

“…Assembly of the three microsyntenic blocks into the deuterostome pharyngeal gene cluster likely contributes to the co-regulation of the genes. Indeed, analysis of the temporal expression profiles using available transcriptomic datasets support the idea that clustering of the pharyngeal genes likely contributes to their co-regulation 50 .…”

“…Second, the protein sequences from other species, including mouse, chick, zebrafish, spotted gar, sea lamprey, amphioxus, ascidian, sea urchin and sea anemone, were aligned to the PFL genome assembly using GeMoMa (version 1.7) 59 . Third, the Illumina RNA-seq short reads from PFL at 16 stages 50 were mapped using STAR aligner (version 2.7.6a) 60 . The subsequent genome-guided transcript reconstruction was conducted with StringTie (version 2.1.4) 61 and CLASS2 (version 2.1.7) 62 .…”