A Maternal System Initiating the Zygotic Developmental Program through Combinatorial Repression in the Ascidian Embryo

PLoS Genet. 2016 May 6;12(5):e1006045. doi: 10.1371/journal.pgen.1006045. eCollection 2016 May.

Abstract

Maternal factors initiate the zygotic developmental program in animal embryos. In embryos of the chordate, Ciona intestinalis, three maternal factors-Gata.a, β-catenin, and Zic-r.a-are required to establish three domains of gene expression at the 16-cell stage; the animal hemisphere, vegetal hemisphere, and posterior vegetal domains. Here, we show how the maternal factors establish these domains. First, only β-catenin and its effector transcription factor, Tcf7, are required to establish the vegetal hemisphere domain. Second, genes specifically expressed in the posterior vegetal domain have additional repressive cis-elements that antagonize the activity of β-catenin/Tcf7. This antagonizing activity is suppressed by Zic-r.a, which is specifically localized in the posterior vegetal domain and binds to DNA indirectly through the interaction with Tcf7. Third, Gata.a directs specific gene expression in the animal hemisphere domain, because β-catenin/Tcf7 weakens the Gata.a-binding activity for target sites through a physical interaction in the vegetal cells. Thus, repressive regulation through protein-protein interactions among the maternal transcription factors is essential to establish the first distinct domains of gene expression in the chordate embryo.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blastomeres / metabolism
  • Body Patterning / genetics
  • Ciona intestinalis / genetics
  • Ciona intestinalis / growth & development
  • Embryonic Development / genetics*
  • GATA Transcription Factors / biosynthesis
  • GATA Transcription Factors / genetics
  • Gene Expression Regulation, Developmental
  • In Situ Hybridization
  • Protein Interaction Maps
  • Sequence Analysis, DNA
  • T Cell Transcription Factor 1 / biosynthesis
  • T Cell Transcription Factor 1 / genetics*
  • Zygote / growth & development*
  • Zygote / metabolism
  • beta Catenin / biosynthesis
  • beta Catenin / genetics*

Substances

  • GATA Transcription Factors
  • T Cell Transcription Factor 1
  • beta Catenin

Grants and funding

This research was supported by Grants-in-Aid from the Japanese Ministry of Education, Culture, Sports, Science and Technology and the Japan Society for the Promotion of Science to YS (25118510; 15k14447) and IOI (25–40065) (https://www.jsps.go.jp/english/index.html), and a CREST program of Japan Science and Technology Agency (JST) (http://www.jst.go.jp/EN/index.html) to YS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.