title: Independent recruitments of a translational regulator in the evolution of self-fertile nematodes.
abstract: Pleiotropic developmental regulators have been repeatedly linked to the evolution of anatomical novelties. Known mechanisms include cis-regulatory DNA changes that alter regulator transcription patterns or modify target-gene linkages. Here, we examine the role of another form of regulation, translational control, in the repeated evolution of self-fertile hermaphroditism in Caenorhabditis nematodes. Caenorhabditis elegans hermaphrodites initiate spermatogenesis in an otherwise female body through translational repression of the gene tra-2. This repression is mediated by GLD-1, an RNA-binding protein also required for oocyte meiosis and differentiation. By contrast, we show that in the convergently hermaphroditic Caenorhabditis briggsae, GLD-1 acts to promote oogenesis. The opposite functions of gld-1 in these species are not gene-intrinsic, but instead result from the unique contexts for its action that evolved in each. In C. elegans, GLD-1 became essential for promoting XX spermatogenesis via changes in the tra-2 mRNA and evolution of the species-specific protein FOG-2. C. briggsae GLD-1 became an essential repressor of sperm-promoting genes, including Cbr-puf-8, and did not evolve a strong association with tra-2. Despite its variable roles in sex determination, the function of gld-1 in female meiotic progression is ancient and conserved. This conserved role may explain why gld-1 is repeatedly recruited to regulate hermaphroditism. We conclude that, as with transcription factors, spatially localized translational regulators play important roles in the evolution of anatomical novelties.
authors: Department of Biology, University of Maryland, College Park, MD 20742, USA.
authors: Alana V
authors: AV
authors: Beadell
authors: Qinwen
authors: Q
authors: Liu
authors: Dorothy M
authors: DM
authors: Johnson
authors: Eric S
authors: ES
authors: Haag
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D002107:Caenorhabditis / Q000145:classification / Q000235:genetics / Q000378:metabolism; D017173:Caenorhabditis elegans / Q000235:genetics* / Q000378:metabolism; D029742:Caenorhabditis elegans Proteins / Q000235:genetics* / Q000378:metabolism; D002454:Cell Differentiation / Q000235:genetics; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism; D019143:Evolution, Molecular; D005260:Female; D005786:Gene Expression Regulation; D005816:Genetic Complementation Test; D057850:Hermaphroditic Organisms / Q000235:genetics / Q000378:metabolism; D015151:Immunoblotting; D008297:Male; D008565:Membrane Proteins / Q000235:genetics / Q000378:metabolism; D008969:Molecular Sequence Data; D009154:Mutation; D009865:Oocytes / Q000166:cytology / Q000378:metabolism; D010802:Phylogeny; D014176:Protein Biosynthesis; D034622:RNA Interference; D020133:Reverse Transcriptase Polymerase Chain Reaction; D017386:Sequence Homology, Amino Acid; D013045:Species Specificity; D013091:Spermatogenesis / Q000235:genetics; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism
chemical_list: D029742:Caenorhabditis elegans Proteins; D004268:DNA-Binding Proteins; C094448:GLD-1 protein, C elegans; D008565:Membrane Proteins; D014157:Transcription Factors; C492171:fog-2 protein, C elegans; C076107:tra-2 protein, C elegans