Independent recruitment of F box genes to regulate hermaphrodite development during nematode evolution

Curr Biol. 2009 Nov 17;19(21):1853-60. doi: 10.1016/j.cub.2009.09.042. Epub 2009 Oct 15.

Abstract

Elucidating the molecular mechanisms that created ancient complex traits like insect wings is difficult. Fortunately, some complex traits have arisen recently. For example, hermaphroditic reproduction evolved independently many times during recent nematode evolution. Although C. elegans hermaphrodites require fog-2, which encodes an F box protein that regulates the translation of tra-2 mRNAs, the related species C. briggsae lacks fog-2. We identified a critical regulator of hermaphrodite development in C. briggsae, named she-1. Analysis of double mutants indicates that she-1 acts upstream of tra-2 in C. briggsae, just as fog-2 does in C. elegans. Molecular cloning shows that she-1 encodes a novel F box protein that was created by a recent gene duplication. Whereas FOG-2 acts through GLD-1 in C. elegans, SHE-1 does not bind GLD-1 in C. briggsae. Thus, both species recruited F box genes produced by recent duplication events into the sex-determination pathway to control hermaphrodite development, but these genes have distinct activities. This result implies that some gene families are more likely to give rise to novel regulatory genes than other families. Finally, we note that null mutations of she-1 are temperature sensitive, so C. briggsae might once have been a facultative hermaphrodite.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Biological Evolution*
  • Caenorhabditis / genetics
  • Caenorhabditis / growth & development
  • Caenorhabditis / physiology*
  • Caenorhabditis elegans Proteins / chemistry
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Caenorhabditis elegans Proteins / physiology
  • Cell Differentiation
  • Chromosome Mapping
  • DNA-Binding Proteins / chemistry
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / physiology
  • Disorders of Sex Development / genetics
  • F-Box Proteins / chemistry
  • F-Box Proteins / genetics
  • F-Box Proteins / physiology*
  • Gene Duplication
  • Helminth Proteins / genetics
  • Helminth Proteins / metabolism
  • Helminth Proteins / physiology*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Membrane Proteins / physiology
  • Models, Genetic
  • Molecular Sequence Data
  • Polymorphism, Single Nucleotide
  • SKP Cullin F-Box Protein Ligases / metabolism
  • Sequence Alignment
  • Sex Determination Processes*
  • Spermatogenesis / genetics
  • Transcription Factors / chemistry
  • Transcription Factors / genetics
  • Transcription Factors / physiology
  • Two-Hybrid System Techniques

Substances

  • Caenorhabditis elegans Proteins
  • DNA-Binding Proteins
  • F-Box Proteins
  • GLD-1 protein, C elegans
  • Helminth Proteins
  • Membrane Proteins
  • Transcription Factors
  • fog-2 protein, C elegans
  • tra-2 protein, C elegans
  • SKP Cullin F-Box Protein Ligases