Transcriptional control and patterning of the pho-1 gene, an essential acid phosphatase expressed in the C. elegans intestine

Dev Biol. 2005 Mar 15;279(2):446-61. doi: 10.1016/j.ydbio.2004.12.012.

Abstract

We have previously described an acid phosphatase enzyme, PHO-1, present at the lumenal surface of all but the anterior six cells of the Caenorhabditis elegans intestine. In the present paper, we identify the pho-1 structural gene, which encodes a histidine acid phosphatase showing highest similarity to human prostatic acid phosphatase. The pho-1 5'-flanking DNA is capable of directing reporter gene expression that is both gut specific, correctly timed and correctly "patterned", that is, not expressed in the gut anterior. Furthermore, this anterior-posterior patterning of pho-1 expression responds to the C. elegans Wnt pathway as if pho-1 is repressed (directly or indirectly) by high levels of the HMG effector protein POP-1. Transgenic analysis of the pho-1 promoter shows that gut expression is critically dependent on a single WGATAR site. The gut-specific GATA factor ELT-2 binds to this site in vitro and removal of ELT-2 from the embryo destroys expression of the pho-1 reporter. Thus, all our results indicate that pho-1 is a direct downstream target of ELT-2. Finally, the pho-1 loss-of-function mutation shows an interesting and unexpected phenotype for a somatically-expressed hydrolytic enzyme: loss of pho-1 causes arrest of the majority of embryos but this lethality is a maternal effect. We suggest that pho-1 is required by the maternal intestine to assimilate some nutrient or cleavage product that is subsequently provided to the next generation of embryos.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acid Phosphatase* / genetics*
  • Acid Phosphatase* / metabolism*
  • Amino Acid Sequence
  • Animals
  • Animals, Genetically Modified
  • Body Patterning*
  • Caenorhabditis elegans Proteins* / genetics*
  • Caenorhabditis elegans Proteins* / metabolism*
  • Caenorhabditis elegans* / anatomy & histology
  • Caenorhabditis elegans* / enzymology
  • Caenorhabditis elegans* / genetics
  • Cell Lineage
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • GATA Transcription Factors
  • Gene Expression Regulation, Developmental*
  • Genes, Reporter
  • High Mobility Group Proteins / genetics
  • High Mobility Group Proteins / metabolism
  • Humans
  • Intestines / cytology
  • Intestines / embryology
  • Intestines / enzymology*
  • Molecular Sequence Data
  • Phenotype
  • RNA Interference
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Sequence Alignment
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transcription, Genetic*

Substances

  • Caenorhabditis elegans Proteins
  • DNA-Binding Proteins
  • ELT-2 protein, C elegans
  • GATA Transcription Factors
  • High Mobility Group Proteins
  • Recombinant Fusion Proteins
  • Transcription Factors
  • pop-1 protein, C elegans
  • Acid Phosphatase
  • PHO-1 protein, C elegans