Recapitulation-like developmental transitions of chromatin accessibility in vertebrates

Masahiro Uesaka,Shigeru Kuratani,Naoki Irie,Hiroyuki Takeda

doi:10.1186/s40851-019-0148-9

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.

Highlights

Animal embryogenesis generally proceeds from a simple, single-celled zygote to a complex, multicellular organism
The ATAC-seq reads were enriched at the transcription start sites (TSSs) of genes with low background noise, and the read enrichment profiles differed across developmental stages (Fig. 1a)
The genomic distribution of accessible chromatin regions (ACRs) was similar to that reported in previous studies [26, 27] (Additional file 2: Figure S2); ACRs were significantly enriched at promoters, with the majority mapped to intergenic regions or introns (Additional file 2: Figure S2)

Summary

Introduction

Animal embryogenesis generally proceeds from a simple, single-celled zygote to a complex, multicellular organism. Previous studies based on the expression profiling of protein-coding genes during embryogenesis have tried to detect potential parallelisms between development and evolution, such as possible shifts of the conserved midembryonic stages to later stages when analyzed at smaller evolutionary scales [4, 7, 8]. None of these studies detected later recapitulative patterns in mid-to-late embryogenesis [4,5,6,7,8], instead supporting persistent conservation of the mid-embryonic stages [8, 17, 18]. It should be noted that repeated recruitment of the same protein-coding genes at different developmental stages [8] would obscure any recapitulative pattern, which highlights the importance of using alternative experimental approaches to examine evolutionary changes in gene expression regulation that occurred along a phylogenetic trajectory

Methods

Results

Conclusion