Skip to main content
Genetics logoLink to Genetics
. 1999 May;152(1):209–220. doi: 10.1093/genetics/152.1.209

spe-12 encodes a sperm cell surface protein that promotes spermiogenesis in Caenorhabditis elegans.

J Nance 1, A N Minniti 1, C Sadler 1, S Ward 1
PMCID: PMC1460590  PMID: 10224255

Abstract

During spermiogenesis, Caenorhabditis elegans spermatids activate and mature into crawling spermatozoa without synthesizing new proteins. Mutations in the spe-12 gene block spermatid activation, rendering normally self-fertile hermaphrodites sterile. Mutant males, however, are fertile. Surprisingly, when mutant hermaphrodites mate with a male, their self-spermatids activate and form functional spermatozoa, presumably due to contact with male seminal fluid. Here we show that, in addition to its essential role in normal activation of hermaphrodite-derived spermatids, SPE-12 also plays a supplementary but nonessential role in mating-induced activation. We have identified the spe-12 gene, which encodes a novel protein containing a single transmembrane domain. spe-12 mRNA is expressed in the sperm-producing germ line and the protein localizes to the spermatid cell surface. We propose that SPE-12 functions downstream of both hermaphrodite- and male-derived activation signals in a spermatid signaling pathway that initiates spermiogenesis.

Full Text

The Full Text of this article is available as a PDF (294.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Achanzar W. E., Ward S. A nematode gene required for sperm vesicle fusion. J Cell Sci. 1997 May;110(Pt 9):1073–1081. doi: 10.1242/jcs.110.9.1073. [DOI] [PubMed] [Google Scholar]
  2. Argon Y., Ward S. Caenorhabditis elegans fertilization-defective mutants with abnormal sperm. Genetics. 1980 Oct;96(2):413–433. doi: 10.1093/genetics/96.2.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974 May;77(1):71–94. doi: 10.1093/genetics/77.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burke D. J., Ward S. Identification of a large multigene family encoding the major sperm protein of Caenorhabditis elegans. J Mol Biol. 1983 Nov 25;171(1):1–29. doi: 10.1016/s0022-2836(83)80312-x. [DOI] [PubMed] [Google Scholar]
  5. Church D. L., Guan K. L., Lambie E. J. Three genes of the MAP kinase cascade, mek-2, mpk-1/sur-1 and let-60 ras, are required for meiotic cell cycle progression in Caenorhabditis elegans. Development. 1995 Aug;121(8):2525–2535. doi: 10.1242/dev.121.8.2525. [DOI] [PubMed] [Google Scholar]
  6. Déry O., Corvera C. U., Steinhoff M., Bunnett N. W. Proteinase-activated receptors: novel mechanisms of signaling by serine proteases. Am J Physiol. 1998 Jun;274(6 Pt 1):C1429–C1452. doi: 10.1152/ajpcell.1998.274.6.C1429. [DOI] [PubMed] [Google Scholar]
  7. Han M., Sternberg P. W. let-60, a gene that specifies cell fates during C. elegans vulval induction, encodes a ras protein. Cell. 1990 Nov 30;63(5):921–931. doi: 10.1016/0092-8674(90)90495-z. [DOI] [PubMed] [Google Scholar]
  8. Hodgkin J., Horvitz H. R., Brenner S. Nondisjunction Mutants of the Nematode CAENORHABDITIS ELEGANS. Genetics. 1979 Jan;91(1):67–94. doi: 10.1093/genetics/91.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ihle J. N. Cytokine receptor signalling. Nature. 1995 Oct 19;377(6550):591–594. doi: 10.1038/377591a0. [DOI] [PubMed] [Google Scholar]
  10. Kayne P. S., Sternberg P. W. Ras pathways in Caenorhabditis elegans. Curr Opin Genet Dev. 1995 Feb;5(1):38–43. doi: 10.1016/s0959-437x(95)90051-9. [DOI] [PubMed] [Google Scholar]
  11. King K. L., Essig J., Roberts T. M., Moerland T. S. Regulation of the Ascaris major sperm protein (MSP) cytoskeleton by intracellular pH. Cell Motil Cytoskeleton. 1994;27(3):193–205. doi: 10.1002/cm.970270302. [DOI] [PubMed] [Google Scholar]
  12. Kramer J. M., French R. P., Park E. C., Johnson J. J. The Caenorhabditis elegans rol-6 gene, which interacts with the sqt-1 collagen gene to determine organismal morphology, encodes a collagen. Mol Cell Biol. 1990 May;10(5):2081–2089. doi: 10.1128/mcb.10.5.2081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. L'Hernault S. W., Roberts T. M. Cell biology of nematode sperm. Methods Cell Biol. 1995;48:273–301. doi: 10.1016/s0091-679x(08)61392-8. [DOI] [PubMed] [Google Scholar]
  14. L'Hernault S. W., Shakes D. C., Ward S. Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Genetics. 1988 Oct;120(2):435–452. doi: 10.1093/genetics/120.2.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. LaMunyon C. W., Ward S. Assessing the viability of mutant and manipulated sperm by artificial insemination of Caenorhabditis elegans. Genetics. 1994 Nov;138(3):689–692. doi: 10.1093/genetics/138.3.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. LaMunyon C. W., Ward S. Increased competitiveness of nematode sperm bearing the male X chromosome. Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):185–189. doi: 10.1073/pnas.94.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. LaMunyon C. W., Ward S. Sperm precedence in a hermaphroditic nematode (Caenorhabditis elegans) is due to competitive superiority of male sperm. Experientia. 1995 Aug 16;51(8):817–823. doi: 10.1007/BF01922436. [DOI] [PubMed] [Google Scholar]
  18. Mello C. C., Kramer J. M., Stinchcomb D., Ambros V. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991 Dec;10(12):3959–3970. doi: 10.1002/j.1460-2075.1991.tb04966.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Minniti A. N., Sadler C., Ward S. Genetic and molecular analysis of spe-27, a gene required for spermiogenesis in Caenorhabditis elegans hermaphrodites. Genetics. 1996 May;143(1):213–223. doi: 10.1093/genetics/143.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nelson G. A., Lew K. K., Ward S. Intersex, a temperature-sensitive mutant of the nematode Caenorhabditis elegans. Dev Biol. 1978 Oct;66(2):386–409. doi: 10.1016/0012-1606(78)90247-6. [DOI] [PubMed] [Google Scholar]
  21. Pavalko F. M., Roberts T. M. Posttranslational insertion of a membrane protein on Caenorhabditis elegans sperm occurs without de novo protein synthesis. J Cell Biochem. 1989 Oct;41(2):57–70. doi: 10.1002/jcb.240410203. [DOI] [PubMed] [Google Scholar]
  22. Perrimon N. Signalling pathways initiated by receptor protein tyrosine kinases in Drosophila. Curr Opin Cell Biol. 1994 Apr;6(2):260–266. doi: 10.1016/0955-0674(94)90145-7. [DOI] [PubMed] [Google Scholar]
  23. Sepsenwol S., Taft S. J. In vitro induction of crawling in the amoeboid sperm of the nematode parasite, Ascaris suum. Cell Motil Cytoskeleton. 1990;15(2):99–110. doi: 10.1002/cm.970150206. [DOI] [PubMed] [Google Scholar]
  24. Shakes D. C., Ward S. Mutations that disrupt the morphogenesis and localization of a sperm-specific organelle in Caenorhabditis elegans. Dev Biol. 1989 Aug;134(2):307–316. doi: 10.1016/0012-1606(89)90103-6. [DOI] [PubMed] [Google Scholar]
  25. Simon M. A., Bowtell D. D., Dodson G. S., Laverty T. R., Rubin G. M. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell. 1991 Nov 15;67(4):701–716. doi: 10.1016/0092-8674(91)90065-7. [DOI] [PubMed] [Google Scholar]
  26. Singson A., Mercer K. B., L'Hernault S. W. The C. elegans spe-9 gene encodes a sperm transmembrane protein that contains EGF-like repeats and is required for fertilization. Cell. 1998 Apr 3;93(1):71–79. doi: 10.1016/s0092-8674(00)81147-2. [DOI] [PubMed] [Google Scholar]
  27. Varkey J. P., Muhlrad P. J., Minniti A. N., Do B., Ward S. The Caenorhabditis elegans spe-26 gene is necessary to form spermatids and encodes a protein similar to the actin-associated proteins kelch and scruin. Genes Dev. 1995 May 1;9(9):1074–1086. doi: 10.1101/gad.9.9.1074. [DOI] [PubMed] [Google Scholar]
  28. Ward S., Argon Y., Nelson G. A. Sperm morphogenesis in wild-type and fertilization-defective mutants of Caenorhabditis elegans. J Cell Biol. 1981 Oct;91(1):26–44. doi: 10.1083/jcb.91.1.26. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ward S., Carrel J. S. Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol. 1979 Dec;73(2):304–321. doi: 10.1016/0012-1606(79)90069-1. [DOI] [PubMed] [Google Scholar]
  30. Wassarman D. A., Therrien M., Rubin G. M. The Ras signaling pathway in Drosophila. Curr Opin Genet Dev. 1995 Feb;5(1):44–50. doi: 10.1016/s0959-437x(95)90052-7. [DOI] [PubMed] [Google Scholar]
  31. Weiss A., Littman D. R. Signal transduction by lymphocyte antigen receptors. Cell. 1994 Jan 28;76(2):263–274. doi: 10.1016/0092-8674(94)90334-4. [DOI] [PubMed] [Google Scholar]
  32. Wilson R., Ainscough R., Anderson K., Baynes C., Berks M., Bonfield J., Burton J., Connell M., Copsey T., Cooper J. 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature. 1994 Mar 3;368(6466):32–38. doi: 10.1038/368032a0. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES