The vertebrate phylotypic stage and an early bilaterian-related stage in mouse embryogenesis defined by genomic information

Naoki Irie,Atsuko Sehara-Fujisawa

doi:10.1186/1741-7007-5-1

Abstract

BackgroundEmbryos of taxonomically different vertebrates are thought to pass through a stage in which they resemble one another morphologically. This "vertebrate phylotypic stage" may represent the basic vertebrate body plan that was established in the common ancestor of vertebrates. However, much controversy remains about when the phylotypic stage appears, and whether it even exists. To overcome the limitations of studies based on morphological comparison, we explored a comprehensive quantitative method for defining the constrained stage using expressed sequence tag (EST) data, gene ontologies (GO), and available genomes of various animals. If strong developmental constraints occur during the phylotypic stage of vertebrate embryos, then genes conserved among vertebrates would be highly expressed at this stage.ResultsWe established a novel method for evaluating the ancestral nature of mouse embryonic stages that does not depend on comparative morphology. The numerical "ancestor index" revealed that the mouse indeed has a highly conserved embryonic period at embryonic day 8.0–8.5, the time of appearance of the pharyngeal arch and somites. During this period, the mouse prominently expresses GO-determined developmental genes shared among vertebrates. Similar analyses revealed the existence of a bilaterian-related period, during which GO-determined developmental genes shared among bilaterians are markedly expressed at the cleavage-to-gastrulation period. The genes associated with the phylotypic stage identified by our method are essential in embryogenesis.ConclusionOur results demonstrate that the mid-embryonic stage of the mouse is indeed highly constrained, supporting the existence of the phylotypic stage. Furthermore, this candidate stage is preceded by a putative bilaterian ancestor-related period. These results not only support the developmental hourglass model, but also highlight the hierarchical aspect of embryogenesis proposed by von Baer. Identification of conserved stages and tissues by this method in various animals would be a powerful tool to examine the phylotypic stage hypothesis, and to understand which kinds of developmental events and gene sets are evolutionarily constrained and how they limit the possible variations of animal basic body plans.

Highlights

Embryos of taxonomically different vertebrates are thought to pass through a stage in which they resemble one another morphologically
Estimating the ancestral nature of mouse embryogenesis On the basis that the vertebrate phylotypic stage should express the highest ratio of genes that conceivably existed in ancestral vertebrates, or Vertebrate genes, we established the following index: Vertebrate ancestor index at developmental stage k = Vk/Nk
Similar to the results obtained with genome-level analysis, both of these peaks were earlier than the putative vertebrate phylotypic stage, spanning from the period of cleavage to the onset of gastrulation (Table 1). These results suggest that this early embryonic period carries the basic body plan of bilaterians, making it the "bilateriotypic" stage

Summary

Introduction

Embryos of taxonomically different vertebrates are thought to pass through a stage in which they resemble one another morphologically. In 1828, Karl von Baer was the first to describe revolutionary laws for animal development [1], inferring that the later the stage of embryogenesis of related organisms, the less they resemble each other [1,2] This "progressive divergence model" was challenged by Seidel, Sander, and Elinson [3,4,5], who noted that earlier stages of development (such as patterns of cleavage) have relatively divergent morphological patterns among species, and so do not always fit the rule. A few detailed morphological studies have thrown doubt on the existence of a phylotypic stage [13,14] These problems are due mainly to the difficulty in evaluating conserved or constrained developmental stages by morphological resemblance. The problem of heterochrony prevents us from concluding whether each vertebrate really has a phylotypic stage, and whether any morphological features are associated with the stage

Methods

Results

Conclusion