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COMP-1 promotes competitive advantage of nematode sperm.

Hansen JM, Chavez DR, Stanfield GM - Elife (2015)

Bottom Line: In this study, we utilize a forward genetic screen in Caenorhabditis elegans to identify a gene, comp-1, whose function is specifically required in competitive contexts.We show that comp-1 functions in sperm to modulate their migration through and localization within the reproductive tract, thereby promoting their access to oocytes.Contrary to previously described models, comp-1 mutant sperm show no defects in size or velocity, thereby defining a novel pathway for preferential usage.

View Article: PubMed Central - PubMed

Affiliation: Department of Human Genetics, University of Utah, Salt Lake City, United States.

ABSTRACT
Competition among sperm to fertilize oocytes is a ubiquitous feature of sexual reproduction as well as a profoundly important aspect of sexual selection. However, little is known about the cellular mechanisms sperm use to gain competitive advantage or how these mechanisms are regulated genetically. In this study, we utilize a forward genetic screen in Caenorhabditis elegans to identify a gene, comp-1, whose function is specifically required in competitive contexts. We show that comp-1 functions in sperm to modulate their migration through and localization within the reproductive tract, thereby promoting their access to oocytes. Contrary to previously described models, comp-1 mutant sperm show no defects in size or velocity, thereby defining a novel pathway for preferential usage. Our results indicate not only that sperm functional traits can influence the outcome of sperm competition, but also that these traits can be modulated in a context-dependent manner depending on the presence of competing sperm.

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A COMP-1::GFP transgene rescues the male precedence defects of comp-1 mutants.Expression of COMP-1::GFP rescues the precedence defect. comp-1(gk1149); jnSi171[Pcomp-1::COMP-1::GFP] males have a wild-type precedence pattern in crosses to dpy-4 hermaphrodites. Precedence assays were performed as in Figure 1D. ***, p < 0.001; **, p < 0.01; ns, not significant (Kolmogorov–Smirnov test). Lines indicate medians. In addition to the indicated genotypes, control strains contained the transgene oxSi221[Peft-3 ::GFP].DOI:http://dx.doi.org/10.7554/eLife.05423.014
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fig4s1: A COMP-1::GFP transgene rescues the male precedence defects of comp-1 mutants.Expression of COMP-1::GFP rescues the precedence defect. comp-1(gk1149); jnSi171[Pcomp-1::COMP-1::GFP] males have a wild-type precedence pattern in crosses to dpy-4 hermaphrodites. Precedence assays were performed as in Figure 1D. ***, p < 0.001; **, p < 0.01; ns, not significant (Kolmogorov–Smirnov test). Lines indicate medians. In addition to the indicated genotypes, control strains contained the transgene oxSi221[Peft-3 ::GFP].DOI:http://dx.doi.org/10.7554/eLife.05423.014

Mentions: To determine the localization of COMP-1, we generated worm strains expressing transgenes that contained the full-length comp-1 coding region fused to either mCherry or GFP. Worms carrying the GFP fusion showed rescue of the male precedence defect, suggesting that the fluorescent tags did not interfere with protein function or localization (Figure 4—figure supplement 1 and data not shown). The COMP-1 fusion proteins displayed a punctate pattern in the cytoplasm of both developing spermatids and mature sperm, where they were restricted to the cell body region (Figure 4E–F and data not shown). These punctae were visible in sperm from both males and hermaphrodites (Figure 4 and data not shown). To determine whether the COMP-1 protein was localized to a specific subcellular location, we performed co-labeling experiments with the vital dye Mitotracker, a marker of mitochondria, and PEEL-1::GFP, which labels the sperm-specific membranous organelles (MOs) (Chen et al., 2000; Seidel et al., 2011). We also examined the phosphatase GSP-3/4, which is involved in cytoskeletal dynamics and shows polarized localization within the pseudopod (Wu et al., 2011). COMP-1 did not colocalize with any of these markers of sperm structure or with the sperm nucleus (Figure 4E–P), and its absence from the pseudopod suggests that it is not involved directly with cellular locomotion, at least by modulating cytoskeletal dynamics.


COMP-1 promotes competitive advantage of nematode sperm.

Hansen JM, Chavez DR, Stanfield GM - Elife (2015)

A COMP-1::GFP transgene rescues the male precedence defects of comp-1 mutants.Expression of COMP-1::GFP rescues the precedence defect. comp-1(gk1149); jnSi171[Pcomp-1::COMP-1::GFP] males have a wild-type precedence pattern in crosses to dpy-4 hermaphrodites. Precedence assays were performed as in Figure 1D. ***, p < 0.001; **, p < 0.01; ns, not significant (Kolmogorov–Smirnov test). Lines indicate medians. In addition to the indicated genotypes, control strains contained the transgene oxSi221[Peft-3 ::GFP].DOI:http://dx.doi.org/10.7554/eLife.05423.014
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4400581&req=5

fig4s1: A COMP-1::GFP transgene rescues the male precedence defects of comp-1 mutants.Expression of COMP-1::GFP rescues the precedence defect. comp-1(gk1149); jnSi171[Pcomp-1::COMP-1::GFP] males have a wild-type precedence pattern in crosses to dpy-4 hermaphrodites. Precedence assays were performed as in Figure 1D. ***, p < 0.001; **, p < 0.01; ns, not significant (Kolmogorov–Smirnov test). Lines indicate medians. In addition to the indicated genotypes, control strains contained the transgene oxSi221[Peft-3 ::GFP].DOI:http://dx.doi.org/10.7554/eLife.05423.014
Mentions: To determine the localization of COMP-1, we generated worm strains expressing transgenes that contained the full-length comp-1 coding region fused to either mCherry or GFP. Worms carrying the GFP fusion showed rescue of the male precedence defect, suggesting that the fluorescent tags did not interfere with protein function or localization (Figure 4—figure supplement 1 and data not shown). The COMP-1 fusion proteins displayed a punctate pattern in the cytoplasm of both developing spermatids and mature sperm, where they were restricted to the cell body region (Figure 4E–F and data not shown). These punctae were visible in sperm from both males and hermaphrodites (Figure 4 and data not shown). To determine whether the COMP-1 protein was localized to a specific subcellular location, we performed co-labeling experiments with the vital dye Mitotracker, a marker of mitochondria, and PEEL-1::GFP, which labels the sperm-specific membranous organelles (MOs) (Chen et al., 2000; Seidel et al., 2011). We also examined the phosphatase GSP-3/4, which is involved in cytoskeletal dynamics and shows polarized localization within the pseudopod (Wu et al., 2011). COMP-1 did not colocalize with any of these markers of sperm structure or with the sperm nucleus (Figure 4E–P), and its absence from the pseudopod suggests that it is not involved directly with cellular locomotion, at least by modulating cytoskeletal dynamics.

Bottom Line: In this study, we utilize a forward genetic screen in Caenorhabditis elegans to identify a gene, comp-1, whose function is specifically required in competitive contexts.We show that comp-1 functions in sperm to modulate their migration through and localization within the reproductive tract, thereby promoting their access to oocytes.Contrary to previously described models, comp-1 mutant sperm show no defects in size or velocity, thereby defining a novel pathway for preferential usage.

View Article: PubMed Central - PubMed

Affiliation: Department of Human Genetics, University of Utah, Salt Lake City, United States.

ABSTRACT
Competition among sperm to fertilize oocytes is a ubiquitous feature of sexual reproduction as well as a profoundly important aspect of sexual selection. However, little is known about the cellular mechanisms sperm use to gain competitive advantage or how these mechanisms are regulated genetically. In this study, we utilize a forward genetic screen in Caenorhabditis elegans to identify a gene, comp-1, whose function is specifically required in competitive contexts. We show that comp-1 functions in sperm to modulate their migration through and localization within the reproductive tract, thereby promoting their access to oocytes. Contrary to previously described models, comp-1 mutant sperm show no defects in size or velocity, thereby defining a novel pathway for preferential usage. Our results indicate not only that sperm functional traits can influence the outcome of sperm competition, but also that these traits can be modulated in a context-dependent manner depending on the presence of competing sperm.

Show MeSH
Related in: MedlinePlus