A catalog of Xenopus tropicalis transcription factors and their regional expression in the early gastrula stage embryo

Abstract

Gene regulatory networks (GRNs) involve highly combinatorial interactions between transcription factors and short sequence motifs in cis-regulatory modules of target genes to control cellular phenotypes. The GRNs specifying most cell types are largely unknown and are the subject of wide interest. A catalog of transcription factors is a valuable tool toward obtaining a deeper understanding of the role of these critical effectors in any biological setting. Here we present a comprehensive catalog of the transcription factors for the diploid frog Xenopus tropicalis. We identify 1235 genes encoding DNA-binding transcription factors, comparable to the numbers found in typical mammalian species. In detail, the repertoire of X. tropicalis transcription factor genes is nearly identical to human and mouse, with the exception of zinc finger family members, and a small number of species/lineage-specific gene duplications and losses relative to the mammalian repertoires. We applied this resource to the identification of transcription factors differentially expressed in the early gastrula stage embryo. We find transcription factor enrichment in Spemann's organizer, the ventral mesoderm, ectoderm and endoderm, and report 218 TFs that show regionalized expression patterns at this stage. Many of these have not been previously reported as expressed in the early embryo, suggesting thus far unappreciated roles for many transcription factors in the GRNs regulating early development. We expect our transcription factor catalog will facilitate myriad studies using Xenopus as a model system to understand basic biology and human disease.

Foxh1 Occupies cis-Regulatory Modules Prior to Dynamic Transcription Factor Interactions Controlling the Mesendoderm Gene Program

“…In Xenopus, Foxh1 mRNA is present in the unfertilized egg (Chen et al, 1996; Howell et al, 2002), and our work in Xenopus tropicalis reveals that Foxh1 mRNA is present equally in animal and vegetal halves of the 8-cell embryo (K.P. and K.W.Y.C, data not shown) and ubiquitously in the early gastrula (Chiu et al, 2014; Blitz et al, in press). Recent high-resolution transcriptome analysis performed using polyA-selected (mRNA-seq) and ribosome-depleted (rdRNA-seq) samples (Owens et al, 2016) reveals that the majority of maternally expressed foxh1 transcripts are non-polyadenylated and undergo rapid polyadenylation shortly after fertilization (Figure 1A, Figure S1A).…”

“…Through mRNA-seq on dissected Xenopus tropicalis embryos, Blitz et al (In press) recently examined the tissue-specific gene expression in the early gastrula embryo. Using these data, we investigated whether genes associated with persistent peaks (‘persistent genes’) have a unique spatial profile compared to all Foxh1-associated genes.…”

Developmentally regulated long non-coding RNAs in Xenopus tropicalis

“…We obtained RNA-seq data from dissected embryonic tissues (animal poles, dorsal, lateral and ventral marginal zones, and vegetal masses, representing ectoderm, dorsal mesoderm, lateral mesoderm, ventral mesoderm and endoderm, respectively) at the gastrula stage (Blitz et al, 2016). Reads from these datasets were mapped to our lncRNA collection identified in this study.…”

“…Stage 10–10.25 gastrula embryos were manually dissected into five fragments representing ectoderm, dorsal mesoderm, lateral mesoderm, ventral mesoderm and endoderm (Blitz et al, 2016) and RNAs were isolated after homogenization. The RNA samples were subjected to polyA+ selection and library production according to the Illumina Tru-Seq mRNA-seq kit.…”

“…The RNA samples were subjected to polyA+ selection and library production according to the Illumina Tru-Seq mRNA-seq kit. Libraries were ligated using bar-coded adaptors and subjected to 50-bp single end sequencing on an Illumina HiSeq2000 instrument (Blitz et al, 2016). Dissection RNA-seq datasets can be found in Blitz et al (2016).…”