A Comparative Analysis of Transcription Factor Expression during Metazoan Embryonic Development

Alicia N Schep,Boris Adryan,Johannes Jaeger

doi:10.1371/journal.pone.0066826

Alicia N Schep, Boris Adryan + Show 1 more

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https://doi.org/10.1371/journal.pone.0066826

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Journal: PLoS ONE	Publication Date: Jun 14, 2013
Citations: 63	License type: CC BY 4.0

Affiliation: University of Cambridge, Stanford University

Abstract

During embryonic development, a complex organism is formed from a single starting cell. These processes of growth and differentiation are driven by large transcriptional changes, which are following the expression and activity of transcription factors (TFs). This study sought to compare TF expression during embryonic development in a diverse group of metazoan animals: representatives of vertebrates (Danio rerio, Xenopus tropicalis), a chordate (Ciona intestinalis) and invertebrate phyla such as insects (Drosophila melanogaster, Anopheles gambiae) and nematodes (Caenorhabditis elegans) were sampled, The different species showed overall very similar TF expression patterns, with TF expression increasing during the initial stages of development. C2H2 zinc finger TFs were over-represented and Homeobox TFs were under-represented in the early stages in all species. We further clustered TFs for each species based on their quantitative temporal expression profiles. This showed very similar TF expression trends in development in vertebrate and insect species. However, analysis of the expression of orthologous pairs between more closely related species showed that expression of most individual TFs is not conserved, following the general model of duplication and diversification. The degree of similarity between TF expression between Xenopus tropicalis and Danio rerio followed the hourglass model, with the greatest similarity occuring during the early tailbud stage in Xenopus tropicalis and the late segmentation stage in Danio rerio. However, for Drosophila melanogaster and Anopheles gambiae there were two periods of high TF transcriptome similarity, one during the Arthropod phylotypic stage at 8–10 hours into Drosophila development and the other later at 16–18 hours into Drosophila development.

Highlights

During metazoan embryonic development, a single cell grows, divides, and differentiates into a complex organism with numerous distinct tissues
The pattern of transcription factors (TFs) expression and TF family utilization throughout development appears to be largely similar in a diverse group of species including two vertebrates (Xenopus tropicalis and Danio rerio) and four invertebrates (Ciona intestinalis, Caenorhabditis elegans, Anopheles gambiae and Drosophila melanogaster)
The trend of high utilization of C2H2 zinc finger TFs and low utilization of Homeobox TFs early in development with Homeobox TF utilization increasing later in development described by Adryan and Teichmann (2010) for Drosophila melanogaster can be observed in the five other species considered in this study

Summary

Introduction

A single cell grows, divides, and differentiates into a complex organism with numerous distinct tissues. Microarrays, and more recently RNA-seq have been used to monitor gene expression over the course of development in a variety of model organisms and some non-model organisms as well [3,4,5,6,7,8,9,10,11,12,13,14,15,16,17,18] These studies have shown that embryonic development is characterized by expression changes of most transcripts [4,11,12,13,19,20]. Groups of genes can be clustered together based on when they change expression [4,13,14,15]

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