Roles of the Wnt effector POP-1/TCF in the C. elegans endomesoderm specification gene network

Dev Biol. 2010 Apr 15;340(2):209-21. doi: 10.1016/j.ydbio.2009.09.042. Epub 2009 Oct 7.

Abstract

In C. elegans the 4-cell stage blastomere EMS is an endomesodermal precursor. Its anterior daughter, MS, makes primarily mesodermal cells, while its posterior daughter E generates the entire intestine. The gene regulatory network underlying specification of MS and E has been the subject of study for more than 15 years. A key component of the specification of the two cells is the involvement of the Wnt/beta-catenin asymmetry pathway, which through its nuclear effector POP-1, specifies MS and E as different from each other. Loss of pop-1 function results in the mis-specification of MS as an E-like cell, because POP-1 directly represses the end-1 and end-3 genes in MS, which would otherwise promote an endoderm fate. A long-standing question has been whether POP-1 plays a role in specifying MS fate beyond repression of endoderm fate. This question has been difficult to ask because the only chromosomal lesions that remove both end-1 and end-3 are large deletions removing hundreds of genes. Here, we report the construction of bona fide end-1 end-3 double mutants. In embryos lacking activity of end-1, end-3 and pop-1 together, we find that MS fate is partially restored, while E expresses early markers of MS fate and adopts characteristics of both MS and C. Our results suggest that POP-1 is not critical for MS specification beyond repression of endoderm specification, and reveal that Wnt-modified POP-1 and END-1/3 further reinforce E specification by repressing MS fate in E. By comparison, a previous work suggested that in the related nematode C. briggsae, Cb-POP-1 is not required to repress endoderm specification in MS, in direct contrast with Ce-POP-1, but is critical for repression of MS fate in E. The findings reported here shed new light on the flexibility of combinatorial control mechanisms in endomesoderm specification in Caenorhabditis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans / embryology*
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / metabolism*
  • DNA-Binding Proteins / metabolism*
  • Embryo, Nonmammalian / metabolism
  • Endoderm / metabolism*
  • Gene Expression Regulation, Developmental
  • Gene Regulatory Networks*
  • Genes, Helminth
  • High Mobility Group Proteins / metabolism*
  • Mesoderm / metabolism*
  • Models, Biological
  • Mutation
  • Transcription Factors / metabolism
  • Wnt Proteins / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • DNA-Binding Proteins
  • High Mobility Group Proteins
  • Transcription Factors
  • Wnt Proteins
  • pop-1 protein, C elegans