POP-1 controls axis formation during early gonadogenesis in C. elegans

Development. 2002 Jan;129(2):443-53.

Abstract

The shape and polarity of the C. elegans gonad is defined during early gonadogenesis by two somatic gonadal precursor cells, Z1 and Z4, and their descendants. Z1 and Z4 divide asymmetrically to establish the proximal-distal axes of the gonad and to generate regulatory leader cells that control organ shape. In this paper, we report that pop-1, the C. elegans TCF/LEF-1 transcription factor, controls the first Z1/Z4 asymmetric division and hence controls proximal-distal axis formation. We have identified two pop-1(Sys) alleles (for symmetrical sisters) that render the Z1/Z4 divisions symmetrical. The pop-1(q645) allele is fully penetrant for the Sys gonadogenesis defect in hermaphrodites, but affects male gonads weakly; pop-1(q645) alters a conserved amino acid in the beta-catenin binding domain. The pop-1(q624) allele is weakly penetrant for multiple defects and appears to be a partial loss-of-function mutation; pop-1(q624) alters a conserved amino acid in the HMG-box DNA binding domain. Zygotic pop-1(RNAi) confirms the role of pop-1 in Z1/Z4 asymmetry and reveals additional roles of pop-1, including one in leader cell migration. Two other Wnt pathway regulators, wrm-1 and lit-1, have the same effect as pop-1 on Z1/Z4 asymmetry. Therefore, wrm-1 and lit-1 are required for pop-1 function, rather than opposing it as observed in the early embryo. We conclude that POP-1 controls the Z1/Z4 asymmetric division and thereby establishes the proximal-distal axes of the gonad. This control over proximal-distal polarity extends our view of Wnt signaling in C. elegans, which had previously been known to control anterior-posterior polarities.

Publication types

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

MeSH terms

  • Alleles
  • Amino Acid Sequence
  • Animals
  • Body Patterning*
  • Caenorhabditis elegans / embryology*
  • Caenorhabditis elegans Proteins / chemistry
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Cell Division / physiology*
  • Cell Lineage
  • Cytoskeletal Proteins / metabolism
  • DNA-Binding Proteins / chemistry
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Disorders of Sex Development
  • Gonads / embryology
  • Gonads / growth & development
  • Gonads / physiology
  • High Mobility Group Proteins / chemistry
  • High Mobility Group Proteins / genetics
  • High Mobility Group Proteins / metabolism*
  • Male
  • Membrane Proteins / metabolism
  • Molecular Sequence Data
  • Morphogenesis
  • Pedigree
  • Protein-Serine-Threonine Kinases
  • Proto-Oncogene Proteins / metabolism
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Signal Transduction / physiology
  • Stem Cells / physiology*
  • Transcription Factors / chemistry
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Wnt Proteins
  • Zebrafish Proteins*

Substances

  • Caenorhabditis elegans Proteins
  • Cytoskeletal Proteins
  • DNA-Binding Proteins
  • High Mobility Group Proteins
  • Membrane Proteins
  • Proto-Oncogene Proteins
  • Recombinant Fusion Proteins
  • Transcription Factors
  • WRM-1 protein, C elegans
  • Wnt Proteins
  • Zebrafish Proteins
  • pop-1 protein, C elegans
  • Protein-Serine-Threonine Kinases
  • lit-1 protein, C elegans