Identification of DVA interneuron regulatory sequences in Caenorhabditis elegans

PLoS One. 2013;8(1):e54971. doi: 10.1371/journal.pone.0054971. Epub 2013 Jan 28.

Abstract

Background: The identity of each neuron is determined by the expression of a distinct group of genes comprising its terminal gene battery. The regulatory sequences that control the expression of such terminal gene batteries in individual neurons is largely unknown. The existence of a complete genome sequence for C. elegans and draft genomes of other nematodes let us use comparative genomics to identify regulatory sequences directing expression in the DVA interneuron.

Methodology/principal findings: Using phylogenetic comparisons of multiple Caenorhabditis species, we identified conserved non-coding sequences in 3 of 10 genes (fax-1, nmr-1, and twk-16) that direct expression of reporter transgenes in DVA and other neurons. The conserved region and flanking sequences in an 85-bp intronic region of the twk-16 gene directs highly restricted expression in DVA. Mutagenesis of this 85 bp region shows that it has at least four regions. The central 53 bp region contains a 29 bp region that represses expression and a 24 bp region that drives broad neuronal expression. Two short flanking regions restrict expression of the twk-16 gene to DVA. A shared GA-rich motif was identified in three of these genes but had opposite effects on expression when mutated in the nmr-1 and twk-16 DVA regulatory elements.

Conclusions/significance: We identified by multi-species conservation regulatory regions within three genes that direct expression in the DVA neuron. We identified four contiguous regions of sequence of the twk-16 gene enhancer with positive and negative effects on expression, which combined to restrict expression to the DVA neuron. For this neuron a single binding site may thus not achieve sufficient specificity for cell specific expression. One of the positive elements, an 8-bp sequence required for expression was identified in silico by sequence comparisons of seven nematode species, demonstrating the potential resolution of expanded multi-species phylogenetic comparisons.

Publication types

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

MeSH terms

  • Animals
  • Base Sequence
  • Caenorhabditis elegans / cytology*
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans Proteins / genetics
  • DNA Footprinting
  • DNA Mutational Analysis
  • Enhancer Elements, Genetic / genetics
  • Gene Expression Profiling
  • Genomics
  • Introns / genetics
  • Molecular Sequence Data
  • Neurons / metabolism*
  • Nucleotide Motifs / genetics
  • Phylogeny
  • Regulatory Sequences, Nucleic Acid / genetics*
  • Species Specificity

Substances

  • Caenorhabditis elegans Proteins