Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1997 Jun;146(2):567–581. doi: 10.1093/genetics/146.2.567

The Caenorhabditis Elegans Spe-5 Gene Is Required for Morphogenesis of a Sperm-Specific Organelle and Is Associated with an Inherent Cold-Sensitive Phenotype

K Machaca 1, S W L'Hernault 1
PMCID: PMC1207998  PMID: 9178007

Abstract

The nonrandom segregation of organelles to the appropriate compartment during asymmetric cellular division is observed in many developing systems. Caenorhabditis elegans spermatogenesis is an excellent system to address this issue genetically. The proper progression of spermatogenesis requires specialized intracellular organelles, the fibrous body-membranous organelle complexes (FB-MOs). The FB-MOs play a critical role in cytoplasmic partitioning during the asymmetric cellular division associated with sperm meiosis II. Here we show that spe-5 mutants contain defective, vacuolated FB-MOs and usually arrest spermatogenesis at the spermatocyte stage. Occasionally, spe-5 mutants containing defective FB-MOs will form spermatids that are capable of differentiating into functional spermatozoa. These spe-5 spermatids exhibit an incomplete penetrance for tubulin mis-segregation during the second meiotic division. In addition to morphological and FB-MO segregation defects, all six spe-5 mutants are cold-sensitive, exhibiting a more penetrant sterile phenotype at 16° than 25°. This cold sensitivity could be an inherent property of FB-MO morphogenesis.

Full Text

The Full Text of this article is available as a PDF (7.9 MB).

Selected References

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

  1. Adachi Y., Toda T., Niwa O., Yanagida M. Differential expressions of essential and nonessential alpha-tubulin genes in Schizosaccharomyces pombe. Mol Cell Biol. 1986 Jun;6(6):2168–2178. doi: 10.1128/mcb.6.6.2168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ahringer J. Embryonic tissue differentiation in Caenorhabditis elegans requires dif-1, a gene homologous to mitochondrial solute carriers. EMBO J. 1995 May 15;14(10):2307–2316. doi: 10.1002/j.1460-2075.1995.tb07225.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bazinet C., Villafane R., King J. Novel second-site suppression of a cold-sensitive defect in phage P22 procapsid assembly. J Mol Biol. 1990 Dec 5;216(3):701–716. doi: 10.1016/0022-2836(90)90393-Z. [DOI] [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. 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]
  6. Collins J., Saari B., Anderson P. Activation of a transposable element in the germ line but not the soma of Caenorhabditis elegans. Nature. 1987 Aug 20;328(6132):726–728. doi: 10.1038/328726a0. [DOI] [PubMed] [Google Scholar]
  7. Drubin D. G. Development of cell polarity in budding yeast. Cell. 1991 Jun 28;65(7):1093–1096. doi: 10.1016/0092-8674(91)90001-f. [DOI] [PubMed] [Google Scholar]
  8. Eaton S., Simons K. Apical, basal, and lateral cues for epithelial polarization. Cell. 1995 Jul 14;82(1):5–8. doi: 10.1016/0092-8674(95)90045-4. [DOI] [PubMed] [Google Scholar]
  9. Fane B. A., Hayashi M. Second-site suppressors of a cold-sensitive prohead accessory protein of bacteriophage phi X174. Genetics. 1991 Aug;128(4):663–671. doi: 10.1093/genetics/128.4.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ginés-Candelaria E., Blinkova A., Walker J. R. Mutations in Escherichia coli dnaA which suppress a dnaX(Ts) polymerization mutation and are dominant when located in the chromosomal allele and recessive on plasmids. J Bacteriol. 1995 Feb;177(3):705–715. doi: 10.1128/jb.177.3.705-715.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Golden J. W., Riddle D. L. A pheromone-induced developmental switch in Caenorhabditis elegans: Temperature-sensitive mutants reveal a wild-type temperature-dependent process. Proc Natl Acad Sci U S A. 1984 Feb;81(3):819–823. doi: 10.1073/pnas.81.3.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hartman P. S., Herman R. K. Radiation-sensitive mutants of Caenorhabditis elegans. Genetics. 1982 Oct;102(2):159–178. doi: 10.1093/genetics/102.2.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hirsh D., Oppenheim D., Klass M. Development of the reproductive system of Caenorhabditis elegans. Dev Biol. 1976 Mar;49(1):200–219. doi: 10.1016/0012-1606(76)90267-0. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Hsiao C. L., Black L. W. DNA packaging and the pathway of bacteriophage T4 head assembly. Proc Natl Acad Sci U S A. 1977 Sep;74(9):3652–3656. doi: 10.1073/pnas.74.9.3652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kimura Y., Matsumoto S., Yahara I. Temperature-sensitive mutants of hsp82 of the budding yeast Saccharomyces cerevisiae. Mol Gen Genet. 1994 Mar;242(5):517–527. doi: 10.1007/BF00285275. [DOI] [PubMed] [Google Scholar]
  17. Klass M., Wolf N., Hirsh D. Development of the male reproductive system and sexual transformation in the nematode Caenorhabditis elegans. Dev Biol. 1976 Aug;52(1):1–18. doi: 10.1016/0012-1606(76)90002-6. [DOI] [PubMed] [Google Scholar]
  18. L'Hernault S. W., Arduengo P. M. Mutation of a putative sperm membrane protein in Caenorhabditis elegans prevents sperm differentiation but not its associated meiotic divisions. J Cell Biol. 1992 Oct;119(1):55–68. doi: 10.1083/jcb.119.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. L'Hernault S. W., Benian G. M., Emmons R. B. Genetic and molecular characterization of the Caenorhabditis elegans spermatogenesis-defective gene spe-17. Genetics. 1993 Jul;134(3):769–780. doi: 10.1093/genetics/134.3.769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Levy-Lahad E., Wasco W., Poorkaj P., Romano D. M., Oshima J., Pettingell W. H., Yu C. E., Jondro P. D., Schmidt S. D., Wang K. Candidate gene for the chromosome 1 familial Alzheimer's disease locus. Science. 1995 Aug 18;269(5226):973–977. doi: 10.1126/science.7638622. [DOI] [PubMed] [Google Scholar]
  21. Machaca K., DeFelice L. J., L'Hernault S. W. A novel chloride channel localizes to Caenorhabditis elegans spermatids and chloride channel blockers induce spermatid differentiation. Dev Biol. 1996 May 25;176(1):1–16. doi: 10.1006/dbio.1996.9999. [DOI] [PubMed] [Google Scholar]
  22. McKim K. S., Rose A. M. Chromosome I duplications in Caenorhabditis elegans. Genetics. 1990 Jan;124(1):115–132. doi: 10.1093/genetics/124.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Moir D., Botstein D. Determination of the order of gene function in the yeast nuclear division pathway using cs and ts mutants. Genetics. 1982 Apr;100(4):565–577. doi: 10.1093/genetics/100.4.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mostov K. E., Cardone M. H. Regulation of protein traffic in polarized epithelial cells. Bioessays. 1995 Feb;17(2):129–138. doi: 10.1002/bies.950170208. [DOI] [PubMed] [Google Scholar]
  25. Nabeshima K., Kurooka H., Takeuchi M., Kinoshita K., Nakaseko Y., Yanagida M. p93dis1, which is required for sister chromatid separation, is a novel microtubule and spindle pole body-associating protein phosphorylated at the Cdc2 target sites. Genes Dev. 1995 Jul 1;9(13):1572–1585. doi: 10.1101/gad.9.13.1572. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Oakley B. R., Oakley C. E., Kniepkamp K. S., Rinehart J. E. Isolation and characterization of cold-sensitive mutations at the benA, beta-tubulin, locus of Aspergillus nidulans. Mol Gen Genet. 1985;201(1):56–64. doi: 10.1007/BF00397987. [DOI] [PubMed] [Google Scholar]
  28. Okamoto H., Thomson J. N. Monoclonal antibodies which distinguish certain classes of neuronal and supporting cells in the nervous tissue of the nematode Caenorhabditis elegans. J Neurosci. 1985 Mar;5(3):643–653. doi: 10.1523/JNEUROSCI.05-03-00643.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pogliano K. J., Beckwith J. The Cs sec mutants of Escherichia coli reflect the cold sensitivity of protein export itself. Genetics. 1993 Apr;133(4):763–773. doi: 10.1093/genetics/133.4.763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Roberts T. M., Ward S. Membrane flow during nematode spermiogenesis. J Cell Biol. 1982 Jan;92(1):113–120. doi: 10.1083/jcb.92.1.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rogaev E. I., Sherrington R., Rogaeva E. A., Levesque G., Ikeda M., Liang Y., Chi H., Lin C., Holman K., Tsuda T. Familial Alzheimer's disease in kindreds with missense mutations in a gene on chromosome 1 related to the Alzheimer's disease type 3 gene. Nature. 1995 Aug 31;376(6543):775–778. doi: 10.1038/376775a0. [DOI] [PubMed] [Google Scholar]
  32. Rose A. M., Baillie D. L., Curran J. Meiotic pairing behavior of two free duplications of linkage group I in Caenorhabditis elegans. Mol Gen Genet. 1984;195(1-2):52–56. doi: 10.1007/BF00332723. [DOI] [PubMed] [Google Scholar]
  33. Sale W. S., Besharse J. C., Piperno G. Distribution of acetylated alpha-tubulin in retina and in vitro-assembled microtubules. Cell Motil Cytoskeleton. 1988;9(3):243–253. doi: 10.1002/cm.970090306. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Sherrington R., Rogaev E. I., Liang Y., Rogaeva E. A., Levesque G., Ikeda M., Chi H., Lin C., Li G., Holman K. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature. 1995 Jun 29;375(6534):754–760. doi: 10.1038/375754a0. [DOI] [PubMed] [Google Scholar]
  36. Varkey J. P., Jansma P. L., Minniti A. N., Ward S. The Caenorhabditis elegans spe-6 gene is required for major sperm protein assembly and shows second site non-complementation with an unlinked deficiency. Genetics. 1993 Jan;133(1):79–86. doi: 10.1093/genetics/133.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. 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]
  39. Wu Y., Han M. Suppression of activated Let-60 ras protein defines a role of Caenorhabditis elegans Sur-1 MAP kinase in vulval differentiation. Genes Dev. 1994 Jan;8(2):147–159. doi: 10.1101/gad.8.2.147. [DOI] [PubMed] [Google Scholar]
  40. Zimmermann A., Schaer J. C., Muller D. E., Schneider J., Miodonski-Maculewicz N. M., Schindler R. Formation of mast cell granules in cell cycle mutants of an undifferentiated mastocytoma line: evidence for two different states of reversible proliferative quiescence. J Cell Biol. 1983 Jun;96(6):1756–1760. doi: 10.1083/jcb.96.6.1756. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES