A sensitized genetic background reveals evolution near the terminus of the Caenorhabditis germline sex determination pathway.
Caenorhabditis elegans and Caenorhabditis briggsae are both self-fertile hermaphroditic nematodes that evolved independently from male/female ancestors. In C. elegans, FEM-1, FEM-2, and FEM-3 specify male fates by promoting proteolysis of the male-repressing transcription factor, TRA-1. Phenotypes of tra-1 and fem mutants are consistent with this simple linear model in the soma, but not in the germline. While both XX and XO tra-1(lf) mutants have functional male somas, they produce both sperm and oocytes. Further, all three tra-1; fem double mutants retain the expected male soma, but make only oocytes (the germline fem phenotype). Thus, a poorly characterized tra-1 activity is important for sustained male spermatogenesis, and the fem genes affect germline sexual fate independently of their role in regulating TRA-1. C. briggsae tra-1 mutants are phenotypically identical to their C. elegans counterparts, while the fem mutants differ in the germline: XX and XO C. elegans fem mutants are true females, but in C. briggsae they are self-fertile hermaphrodites. To further explore how C. briggsae hermaphrodites regulate germline sex, we analyzed Cb-tra-1/Cb-fem interactions. Cb-tra-1 is fully epistatic to Cb-fem-2 in the germline, unlike the orthologous C. elegans combination. In contrast, Cb-fem-3 shifts the Cb-tra-1(lf) germline phenotype to that of a nearly normal hermaphrodite in the context of a male somatic gonad. This suggests that Cb-fem-3 is epistatic to Cb-tra-1(lf) (as in C. elegans), and that the normal control of C. briggsae XX spermatogenesis targets Cb-tra-1-independent factors downstream of Cb-fem-3. The effect of Cb-fem-3(lf) on Cb-tra-1(lf) is not mediated by change in the expression of Cb-fog-3, a likely direct germline target of Cb-tra-1. As Cb-fem-2 and Cb-fem-3 have identical single mutant phenotypes, Cb-tra-1 provides a sensitized background that reveals differences in how they promote male germline development. These results represent another way in which C. briggsae germline sex determination is incongruent with that of the outwardly similar C. elegans.
Hill
Robin Cook
RC
Department of Biology, University of Maryland, College Park, MD 20742, USA.
Haag
Eric S
ES
D000818:Animals; D002107:Caenorhabditis / Q000235:genetics* / Q000502:physiology; D017173:Caenorhabditis elegans / Q000235:genetics* / Q000502:physiology; D029742:Caenorhabditis elegans Proteins / Q000378:metabolism; D004268:DNA-Binding Proteins / Q000378:metabolism; D012734:Disorders of Sex Development; D005260:Female; D008297:Male; D008938:Mitosis; D009866:Oogenesis; D010749:Phosphoprotein Phosphatases / Q000378:metabolism; D019849:Sex Determination Processes; D014157:Transcription Factors / Q000378:metabolism
D029742:Caenorhabditis elegans Proteins; D004268:DNA-Binding Proteins; C403465:FOG-3 protein, C elegans; D014157:Transcription Factors; C075059:fem-3 protein, C elegans; C121025:tra-1 protein, C elegans; C097435:Fem-2 protein, C elegans; D010749:Phosphoprotein Phosphatases