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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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Related in: MedlinePlus

COMP-1 is highly conserved within the Caenorhabditis genus and present in related parasitic species.Alignment of C. elegans COMP-1 with its orthologs from other nematode species. Yellow highlighting represents amino acids conserved with the C. elegans protein. Bars above the sequence indicate the positions of the divergent kinase-like (black) and SH2-like (gray) domains, as predicted in the Conserved Domains Database (Marchler-Bauer et al., 2011); an alternate prediction for the kinase-like domain includes amino acids 123–394 (Manning, 2005). Positions of the me69 and gk1149 alleles are shown in red and blue as in Figure 1E. For C. japonica, C. sinica, and N. americanus, the predicted COMP-1 proteins present in current databases were incomplete or had regions with poor similarity. In each case, examination of sequence from the comp-1 region allowed us to generate new predicted proteins showing similarity across the full-length Ce-COMP-1 and the other orthologs. For C. sinica, we obtained sequence from the comp-1 region, which revealed a minor assembly error in Csp5.Scaffold_00675.g14294.tt (PRJNA194557). For C. japonica, previous annotation (WormBase) of the comp-1 region predicted two overlapping gene models encoding proteins similar to the N and C terminus of COMP-1; our new predicted Cja-COMP-1 fuses JA64544 and CJA40432. For N. americanus, we were able to identify additional exons upstream of the comp-1 gene model predicted from NECAME_15795. Other accession numbers: Acey_s0303.g1899.t2 (PRJNA231479), Cang_2012_03_13_00293.g8644.t2 (PRJNA51225), CBP27128, RP29840, Csp5.Scaffold_00675.g14294.tt (PRJNA194557), Csp11.Scaffold630.g17815.ti (PRJNA53597), HCOI01934100.t1 (PRJEB506).DOI:http://dx.doi.org/10.7554/eLife.05423.004
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fig1s1: COMP-1 is highly conserved within the Caenorhabditis genus and present in related parasitic species.Alignment of C. elegans COMP-1 with its orthologs from other nematode species. Yellow highlighting represents amino acids conserved with the C. elegans protein. Bars above the sequence indicate the positions of the divergent kinase-like (black) and SH2-like (gray) domains, as predicted in the Conserved Domains Database (Marchler-Bauer et al., 2011); an alternate prediction for the kinase-like domain includes amino acids 123–394 (Manning, 2005). Positions of the me69 and gk1149 alleles are shown in red and blue as in Figure 1E. For C. japonica, C. sinica, and N. americanus, the predicted COMP-1 proteins present in current databases were incomplete or had regions with poor similarity. In each case, examination of sequence from the comp-1 region allowed us to generate new predicted proteins showing similarity across the full-length Ce-COMP-1 and the other orthologs. For C. sinica, we obtained sequence from the comp-1 region, which revealed a minor assembly error in Csp5.Scaffold_00675.g14294.tt (PRJNA194557). For C. japonica, previous annotation (WormBase) of the comp-1 region predicted two overlapping gene models encoding proteins similar to the N and C terminus of COMP-1; our new predicted Cja-COMP-1 fuses JA64544 and CJA40432. For N. americanus, we were able to identify additional exons upstream of the comp-1 gene model predicted from NECAME_15795. Other accession numbers: Acey_s0303.g1899.t2 (PRJNA231479), Cang_2012_03_13_00293.g8644.t2 (PRJNA51225), CBP27128, RP29840, Csp5.Scaffold_00675.g14294.tt (PRJNA194557), Csp11.Scaffold630.g17815.ti (PRJNA53597), HCOI01934100.t1 (PRJEB506).DOI:http://dx.doi.org/10.7554/eLife.05423.004

Mentions: The COMP-1 protein contains divergent SH2 and protein kinase-like domains and has been classified within a ‘unique’ subset of C. elegans kinases that do not fall clearly within defined families (Manning, 2005); it also lacks closely related paralogs within the C. elegans genome. It is missing three highly conserved core motifs present in active kinases, including the VAIK motif in the N lobe, the HRD motif in the catalytic loop, and the DFG motif within the activation loop, though it does contain the tripeptide APE motif located within the activation segment (Figure 1—figure supplement 1) (Hanks et al., 1988; Hanks and Hunter, 1995; Manning et al., 2002; Nolen et al., 2004; Marchler-Bauer et al., 2011). The absence of these features suggests that the protein is unlikely to have catalytic activity. The me69 allele is predicted to result in a glycine to arginine change in a residue that is conserved in all other orthologs identified to date. COMP-1 orthologs are present in other Caenorhabditis species as well as in the parasites Haemonchus contortus, Ancylostoma ceylanicum, and Necator americanus (Figure 1—figure supplement 1) (WormBase; Laing et al., 2013; Schwarz et al., 2013; Tang et al., 2014). Although COMP-1 appears to be absent from more distant species (WormBase, and unpublished data), it is present in nematodes that utilize male-female as well as male-hermaphrodite reproductive modes.


COMP-1 promotes competitive advantage of nematode sperm.

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

COMP-1 is highly conserved within the Caenorhabditis genus and present in related parasitic species.Alignment of C. elegans COMP-1 with its orthologs from other nematode species. Yellow highlighting represents amino acids conserved with the C. elegans protein. Bars above the sequence indicate the positions of the divergent kinase-like (black) and SH2-like (gray) domains, as predicted in the Conserved Domains Database (Marchler-Bauer et al., 2011); an alternate prediction for the kinase-like domain includes amino acids 123–394 (Manning, 2005). Positions of the me69 and gk1149 alleles are shown in red and blue as in Figure 1E. For C. japonica, C. sinica, and N. americanus, the predicted COMP-1 proteins present in current databases were incomplete or had regions with poor similarity. In each case, examination of sequence from the comp-1 region allowed us to generate new predicted proteins showing similarity across the full-length Ce-COMP-1 and the other orthologs. For C. sinica, we obtained sequence from the comp-1 region, which revealed a minor assembly error in Csp5.Scaffold_00675.g14294.tt (PRJNA194557). For C. japonica, previous annotation (WormBase) of the comp-1 region predicted two overlapping gene models encoding proteins similar to the N and C terminus of COMP-1; our new predicted Cja-COMP-1 fuses JA64544 and CJA40432. For N. americanus, we were able to identify additional exons upstream of the comp-1 gene model predicted from NECAME_15795. Other accession numbers: Acey_s0303.g1899.t2 (PRJNA231479), Cang_2012_03_13_00293.g8644.t2 (PRJNA51225), CBP27128, RP29840, Csp5.Scaffold_00675.g14294.tt (PRJNA194557), Csp11.Scaffold630.g17815.ti (PRJNA53597), HCOI01934100.t1 (PRJEB506).DOI:http://dx.doi.org/10.7554/eLife.05423.004
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fig1s1: COMP-1 is highly conserved within the Caenorhabditis genus and present in related parasitic species.Alignment of C. elegans COMP-1 with its orthologs from other nematode species. Yellow highlighting represents amino acids conserved with the C. elegans protein. Bars above the sequence indicate the positions of the divergent kinase-like (black) and SH2-like (gray) domains, as predicted in the Conserved Domains Database (Marchler-Bauer et al., 2011); an alternate prediction for the kinase-like domain includes amino acids 123–394 (Manning, 2005). Positions of the me69 and gk1149 alleles are shown in red and blue as in Figure 1E. For C. japonica, C. sinica, and N. americanus, the predicted COMP-1 proteins present in current databases were incomplete or had regions with poor similarity. In each case, examination of sequence from the comp-1 region allowed us to generate new predicted proteins showing similarity across the full-length Ce-COMP-1 and the other orthologs. For C. sinica, we obtained sequence from the comp-1 region, which revealed a minor assembly error in Csp5.Scaffold_00675.g14294.tt (PRJNA194557). For C. japonica, previous annotation (WormBase) of the comp-1 region predicted two overlapping gene models encoding proteins similar to the N and C terminus of COMP-1; our new predicted Cja-COMP-1 fuses JA64544 and CJA40432. For N. americanus, we were able to identify additional exons upstream of the comp-1 gene model predicted from NECAME_15795. Other accession numbers: Acey_s0303.g1899.t2 (PRJNA231479), Cang_2012_03_13_00293.g8644.t2 (PRJNA51225), CBP27128, RP29840, Csp5.Scaffold_00675.g14294.tt (PRJNA194557), Csp11.Scaffold630.g17815.ti (PRJNA53597), HCOI01934100.t1 (PRJEB506).DOI:http://dx.doi.org/10.7554/eLife.05423.004
Mentions: The COMP-1 protein contains divergent SH2 and protein kinase-like domains and has been classified within a ‘unique’ subset of C. elegans kinases that do not fall clearly within defined families (Manning, 2005); it also lacks closely related paralogs within the C. elegans genome. It is missing three highly conserved core motifs present in active kinases, including the VAIK motif in the N lobe, the HRD motif in the catalytic loop, and the DFG motif within the activation loop, though it does contain the tripeptide APE motif located within the activation segment (Figure 1—figure supplement 1) (Hanks et al., 1988; Hanks and Hunter, 1995; Manning et al., 2002; Nolen et al., 2004; Marchler-Bauer et al., 2011). The absence of these features suggests that the protein is unlikely to have catalytic activity. The me69 allele is predicted to result in a glycine to arginine change in a residue that is conserved in all other orthologs identified to date. COMP-1 orthologs are present in other Caenorhabditis species as well as in the parasites Haemonchus contortus, Ancylostoma ceylanicum, and Necator americanus (Figure 1—figure supplement 1) (WormBase; Laing et al., 2013; Schwarz et al., 2013; Tang et al., 2014). Although COMP-1 appears to be absent from more distant species (WormBase, and unpublished data), it is present in nematodes that utilize male-female as well as male-hermaphrodite reproductive modes.

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