fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis.

Somatic and germline sex determination pathways have diverged significantly in animals, making comparisons between taxa difficult. To overcome this difficulty, we compared the genes in the germline sex determination pathways of Caenorhabditis elegans and C. briggsae, two Caenorhabditis species with...

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Main Authors: Sudhir Nayak, Johnathan Goree, Tim Schedl
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2005-01-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.0030006
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spelling doaj-d5de08b8fbc846df8d62652fdf955e852021-07-02T17:09:55ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852005-01-0131e610.1371/journal.pbio.0030006fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis.Sudhir NayakJohnathan GoreeTim SchedlSomatic and germline sex determination pathways have diverged significantly in animals, making comparisons between taxa difficult. To overcome this difficulty, we compared the genes in the germline sex determination pathways of Caenorhabditis elegans and C. briggsae, two Caenorhabditis species with similar reproductive systems and sequenced genomes. We demonstrate that C. briggsae has orthologs of all known C. elegans sex determination genes with one exception: fog-2. Hermaphroditic nematodes are essentially females that produce sperm early in life, which they use for self fertilization. In C. elegans, this brief period of spermatogenesis requires FOG-2 and the RNA-binding protein GLD-1, which together repress translation of the tra-2 mRNA. FOG-2 is part of a large C. elegans FOG-2-related protein family defined by the presence of an F-box and Duf38/FOG-2 homogy domain. A fog-2-related gene family is also present in C. briggsae, however, the branch containing fog-2 appears to have arisen relatively recently in C. elegans, post-speciation. The C-terminus of FOG-2 is rapidly evolving, is required for GLD-1 interaction, and is likely critical for the role of FOG-2 in sex determination. In addition, C. briggsae gld-1 appears to play the opposite role in sex determination (promoting the female fate) while maintaining conserved roles in meiotic progression during oogenesis. Our data indicate that the regulation of the hermaphrodite germline sex determination pathway at the level of FOG-2/GLD-1/tra-2 mRNA is fundamentally different between C. elegans and C. briggsae, providing functional evidence in support of the independent evolution of self-fertile hermaphroditism. We speculate on the convergent evolution of hermaphroditism in Caenorhabditis based on the plasticity of the C. elegans germline sex determination cascade, in which multiple mutant paths yield self fertility.https://doi.org/10.1371/journal.pbio.0030006
collection DOAJ
language English
format Article
sources DOAJ
author Sudhir Nayak
Johnathan Goree
Tim Schedl
spellingShingle Sudhir Nayak
Johnathan Goree
Tim Schedl
fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis.
PLoS Biology
author_facet Sudhir Nayak
Johnathan Goree
Tim Schedl
author_sort Sudhir Nayak
title fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis.
title_short fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis.
title_full fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis.
title_fullStr fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis.
title_full_unstemmed fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis.
title_sort fog-2 and the evolution of self-fertile hermaphroditism in caenorhabditis.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2005-01-01
description Somatic and germline sex determination pathways have diverged significantly in animals, making comparisons between taxa difficult. To overcome this difficulty, we compared the genes in the germline sex determination pathways of Caenorhabditis elegans and C. briggsae, two Caenorhabditis species with similar reproductive systems and sequenced genomes. We demonstrate that C. briggsae has orthologs of all known C. elegans sex determination genes with one exception: fog-2. Hermaphroditic nematodes are essentially females that produce sperm early in life, which they use for self fertilization. In C. elegans, this brief period of spermatogenesis requires FOG-2 and the RNA-binding protein GLD-1, which together repress translation of the tra-2 mRNA. FOG-2 is part of a large C. elegans FOG-2-related protein family defined by the presence of an F-box and Duf38/FOG-2 homogy domain. A fog-2-related gene family is also present in C. briggsae, however, the branch containing fog-2 appears to have arisen relatively recently in C. elegans, post-speciation. The C-terminus of FOG-2 is rapidly evolving, is required for GLD-1 interaction, and is likely critical for the role of FOG-2 in sex determination. In addition, C. briggsae gld-1 appears to play the opposite role in sex determination (promoting the female fate) while maintaining conserved roles in meiotic progression during oogenesis. Our data indicate that the regulation of the hermaphrodite germline sex determination pathway at the level of FOG-2/GLD-1/tra-2 mRNA is fundamentally different between C. elegans and C. briggsae, providing functional evidence in support of the independent evolution of self-fertile hermaphroditism. We speculate on the convergent evolution of hermaphroditism in Caenorhabditis based on the plasticity of the C. elegans germline sex determination cascade, in which multiple mutant paths yield self fertility.
url https://doi.org/10.1371/journal.pbio.0030006
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