Recapitulation-like developmental transitions of chromatin accessibility in vertebrates

Abstract

The relationship between development and evolution has been a central theme in evolutionary developmental biology. Across the vertebrates, the most highly conserved gene expression profiles are found at mid-embryonic, organogenesis stages, whereas those at earlier and later stages are more diverged. This hourglass-like pattern of divergence does not necessarily rule out the possibility that gene expression profiles that are more evolutionarily derived appear at later stages of development; however, no molecular-level evidence of such a phenomenon has been reported. To address this issue, we compared putative gene regulatory elements among different species within a phylum. We made a genome-wide assessment of accessible chromatin regions throughout embryogenesis in three vertebrate species (mouse, chicken, and medaka) and estimated the evolutionary ages of these regions to define their evolutionary origins on the phylogenetic tree. In all the three species, we found that genomic regions tend to become accessible in an order that parallels their phylogenetic history, with evolutionarily newer gene regulations activated at later developmental stages. This tendency was restricted only after the mid-embryonic, phylotypic periods. Our results imply a phylogenetic hierarchy of putative regulatory regions, in which their activation parallels the phylogenetic order of their appearance. One evolutionary mechanism that may explain this phenomenon is that newly introduced regulatory elements are more likely to survive if activated at later stages of embryogenesis. Possible relationships between this phenomenon and the so-called recapitulation are discussed.

Dynamic transcriptional and chromatin accessibility landscape of medaka embryogenesis

“…5F). Further studies using ATAC-seq data from human (Wu et al 2018), mouse, chicken (Uesaka et al 2019), zebrafish (Liu et al 2018) also showed this term enrichment in genes with multiple (>2) distal elements (Supplemental Fig. 16).…”

“…With this tool, users could compare gene models from the Ensembl, RefSeq, PacBio, and IGDB sets, and explore all Illumina and ATAC-seq reads coverage and alignments at any genomic locus at each time points. We also incorporated multiple published medaka omics datasets (Nakamura et al 2014;Tena et al 2014;Ichikawa et al 2017;Marlétaz et al 2018;Uesaka et al 2019). In total, we constructed 100 tracks to present various annotations, reads coverage and alignments in embryonic stages (24) and adult tissues (7) samples, using different technologies including RNA-seq (42), ATAC-seq (21), and histone modifications (13).…”

An irregular hourglass pattern describes the tempo of phenotypic development in placental mammal evolution

“…Whether variation in the timing of developmental processes resembles an hourglass continues to intrigue evolutionary, developmental and molecular biologists [1,[4][5][6][7]9,21]. Given the complexity of developmental processes and the vagaries of atomizing developmental transformations into features coded in a comparative series of many species, it is not surprising that our findings do not reflect a 'perfect' hourglass.…”

“…Recently, the exploration of genome-wide transcriptional activity (i.e. gene expression) across diverse animal and plant taxa revealed temporal trends that were somewhat consistent with the hourglass model [6][7][8][9]. This is perhaps best exemplified by landmark studies that traced gene expression during organogenesis (embryogenesis) in placental mammals [6,8].…”

“…This is perhaps best exemplified by landmark studies that traced gene expression during organogenesis (embryogenesis) in placental mammals [6,8]. Crucially, molecular hourglass hypotheses are predicated upon the existence of high interspecific phenotypic similarity during the phylotypic period [7], though this is rarely crossvalidated via comparisons of embryo morphology across phylogenetically divergent lineages (but see [9]).…”