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. 1996 May;143(1):213–223. doi: 10.1093/genetics/143.1.213

Genetic and Molecular Analysis of Spe-27, a Gene Required for Spermiogenesis in Caenorhabditis Elegans Hermaphrodites

A N Minniti 1, C Sadler 1, S Ward 1
PMCID: PMC1207255  PMID: 8722776

Abstract

Hermaphrodites with mutations in the spe-27 gene are self-sterile, laying only unfertilized eggs; mutant males are fertile. Hermaphrodites make spermatids that fail to activate to crawling spermatozoa so passing oocytes sweep them out of the spermatheca. These spermatids do activate and produce self-progeny if young mutant hermaphrodites are mated by fertile (or sterile) males. Spermatids isolated from either mutant males or hermaphrodites initiate activation in vitro when treated with proteases, but then arrest with spiky membrane projections that resemble those of a normal intermediate in pseudoped formation. These phenotypes are identical to spe-8 and spe-12 mutants. They can be explained if males and hermaphrodites have distinct pathways for spermatid activation, and these three genes are necessary only for the hermaphrodite pathway. Consistent with this model, when spe-27 mutant male spermatids without seminal fluid are artificially inseminated into hermaphrodites, they fail to activate. The spe-27 gene has been isolated, sequenced and its regulatory regions identified. The sequence predicts a 131 amino acid polypeptide that has no striking structural motifs and no resemblance to known proteins. Two of the mutations in spe-27 alter mRNA splicing; a third mutation is a temperature-sensitive missense mutation.

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Selected References

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  1. 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]
  2. Barton M. K., Schedl T. B., Kimble J. Gain-of-function mutations of fem-3, a sex-determination gene in Caenorhabditis elegans. Genetics. 1987 Jan;115(1):107–119. doi: 10.1093/genetics/115.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brenner S., Dove W., Herskowitz I., Thomas R. Genes and development: molecular and logical themes. Genetics. 1990 Nov;126(3):479–486. doi: 10.1093/genetics/126.3.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Caffarelli E., Arese M., Santoro B., Fragapane P., Bozzoni I. In vitro study of processing of the intron-encoded U16 small nucleolar RNA in Xenopus laevis. Mol Cell Biol. 1994 May;14(5):2966–2974. doi: 10.1128/mcb.14.5.2966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chandrasekhar A., Ennis H. L., Soll D. R. Biological and molecular correlates between induced dedifferentiation and spore germination in Dictyostelium. Development. 1992 Oct;116(2):417–425. doi: 10.1242/dev.116.2.417. [DOI] [PubMed] [Google Scholar]
  7. Doniach T., Hodgkin J. A sex-determining gene, fem-1, required for both male and hermaphrodite development in Caenorhabditis elegans. Dev Biol. 1984 Nov;106(1):223–235. doi: 10.1016/0012-1606(84)90077-0. [DOI] [PubMed] [Google Scholar]
  8. Evans T. C., Crittenden S. L., Kodoyianni V., Kimble J. Translational control of maternal glp-1 mRNA establishes an asymmetry in the C. elegans embryo. Cell. 1994 Apr 22;77(2):183–194. doi: 10.1016/0092-8674(94)90311-5. [DOI] [PubMed] [Google Scholar]
  9. Ferguson E. L., Horvitz H. R. The multivulva phenotype of certain Caenorhabditis elegans mutants results from defects in two functionally redundant pathways. Genetics. 1989 Sep;123(1):109–121. doi: 10.1093/genetics/123.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Finney R., Ellis M., Langtimm C., Rosen E., Firtel R., Soll D. R. Gene regulation during dedifferentiation in Dictyostelium discoideum. Dev Biol. 1987 Apr;120(2):561–576. doi: 10.1016/0012-1606(87)90259-4. [DOI] [PubMed] [Google Scholar]
  11. Fire A. Integrative transformation of Caenorhabditis elegans. EMBO J. 1986 Oct;5(10):2673–2680. doi: 10.1002/j.1460-2075.1986.tb04550.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hodgkin J. Genetic sex determination mechanisms and evolution. Bioessays. 1992 Apr;14(4):253–261. doi: 10.1002/bies.950140409. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Nachmias V. T., Yoshida K., Glennon M. C. Lowering pH in blood platelets dissociates myosin phosphorylation from shape change and myosin association with the cytoskeleton. J Cell Biol. 1987 Oct;105(4):1761–1769. doi: 10.1083/jcb.105.4.1761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nelson G. A., Roberts T. M., Ward S. Caenorhabditis elegans spermatozoan locomotion: amoeboid movement with almost no actin. J Cell Biol. 1982 Jan;92(1):121–131. doi: 10.1083/jcb.92.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Nelson G. A., Ward S. Vesicle fusion, pseudopod extension and amoeboid motility are induced in nematode spermatids by the ionophore monensin. Cell. 1980 Feb;19(2):457–464. doi: 10.1016/0092-8674(80)90520-6. [DOI] [PubMed] [Google Scholar]
  18. Prislei S., Michienzi A., Presutti C., Fragapane P., Bozzoni I. Two different snoRNAs are encoded in introns of amphibian and human L1 ribosomal protein genes. Nucleic Acids Res. 1993 Dec 25;21(25):5824–5830. doi: 10.1093/nar/21.25.5824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Roberts T. M., Pavalko F. M., Ward S. Membrane and cytoplasmic proteins are transported in the same organelle complex during nematode spermatogenesis. J Cell Biol. 1986 May;102(5):1787–1796. doi: 10.1083/jcb.102.5.1787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Shakes D. C., Ward S. Initiation of spermiogenesis in C. elegans: a pharmacological and genetic analysis. Dev Biol. 1989 Jul;134(1):189–200. doi: 10.1016/0012-1606(89)90088-2. [DOI] [PubMed] [Google Scholar]
  21. Simons K., Fuller S. D. Cell surface polarity in epithelia. Annu Rev Cell Biol. 1985;1:243–288. doi: 10.1146/annurev.cb.01.110185.001331. [DOI] [PubMed] [Google Scholar]
  22. Simons K., Wandinger-Ness A. Polarized sorting in epithelia. Cell. 1990 Jul 27;62(2):207–210. doi: 10.1016/0092-8674(90)90357-k. [DOI] [PubMed] [Google Scholar]
  23. Tautz D. Redundancies, development and the flow of information. Bioessays. 1992 Apr;14(4):263–266. doi: 10.1002/bies.950140410. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Ward S., Klass M. The location of the major protein in Caenorhabditis elegans sperm and spermatocytes. Dev Biol. 1982 Jul;92(1):203–208. doi: 10.1016/0012-1606(82)90164-6. [DOI] [PubMed] [Google Scholar]
  26. Wolf N., Hirsh D., McIntosh J. R. Spermatogenesis in males of the free-living nematode, Caenorhabditis elegans. J Ultrastruct Res. 1978 May;63(2):155–169. doi: 10.1016/s0022-5320(78)80071-9. [DOI] [PubMed] [Google Scholar]

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