The Testis pp 109-119 | Cite as

Developmental Genetics of Spermatogenesis in the Nematode Caenorhabditis elegans

  • Steven W. L’Hernault
  • Andrew W. Singson
Part of the Serono Symposia USA book series (SERONOSYMP)

Abstract

In both mammals and C. elegans, spermatogenesis is the process where a spermatogonial cell undergoes a series of divisions to produce a highly differentiated cell, the spermatozoon. Spermatogonial cellular divisions are incomplete in mammals so that all subsequent stages occur in a syncitium. The situation is similar in C. elegans, where spermatogonial nuclei initially share a common cytoplasm. Spermatogonial divisions in both mammals and C. elegans are regulated by signaling from gonadal accessory cells. In mammals, this process requires a series of accessory cell types, including Sertoli, peritubular myoid, and Leydig cells (1,2). In contrast, one somatic distal tip cell (Fig. 10.1) regulates exit of spermatogonia from mitosis in C. elegans, and it no longer participates in spermatogenesis after meiosis is initiated (3). Spermatogenesis occurs within a tubular structure in both mammals and C. elegans. Differentiation occurs along the length and across the radius of this tube (the seminiferous tubule) in mammals. The Sertoli accessory cell plays a crucial role in both the linear and radial aspects of mammalian spermatogenesis. At any given time, a single Sertoli cell can be in contact with up to 50 individual, developing germ cells that can be at four different stages of development (4). In each mammalian testis, spermatogenesis occurs within a “ball of yarn” composed of seminiferous tubules that, if unraveled, would be many meters long. The C. elegans gonadal tube is ~400 mm long (Fig. 10.1). and only linear differentiation is observed (5). After initiating meiosis, individual C. elegans spermatogonial cells bud from the syncitial testes and lineally complete development without the aid of accessory cells (6).

Keywords

Agar Cage Gall Peri Hunt 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Skinner MK, Norton JN, Mullaney BP, Rosselli M, Whaley PD, Anthony CT. Cell-cell interactions and the regulation of testis function. Ann N Y Acad Sci 1991; 637: 354 – 63.PubMedCrossRefGoogle Scholar
  2. 2.
    deRooij DG, Grootegoed JA. Spermatogonial stem cells. Curr Opin Cell Biol 1998;10:694–701.CrossRefGoogle Scholar
  3. 3.
    Kimble J, White J. On the control of germ cell development in Caenorhabditis elegans. Dev Biol 1981;81:208–19.PubMedCrossRefGoogle Scholar
  4. 4.
    Weber JE, Russell LD, Wong V, Peterson RN. Three-dimensional reconstruction of a rat Stage V Sertoli cell: II. Morphometry of Sertoli-Sertoli and Sertoli-germ-cell relationships. Am J Anat 1983;167:163–79.PubMedCrossRefGoogle Scholar
  5. 5.
    Hirsh D, Oppenheim D, Klass M. Development of the reproductive system of Caenorhabditis elegans. Dev Biol 1976;49:200–19.PubMedCrossRefGoogle Scholar
  6. 6.
    L’Hernault SW . Spermatogenesis. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, eds. C. Elegans II. Cold Spring Harbor: Cold Spring Harbor Laboratory, 1997:271–94.Google Scholar
  7. 7.
    Okabe M, Ikawa M, Ashkenas J. Gametogenesis ’98: male infertility and the genetics of spermatogenesis. Am J Hum Gen 1998;62:1274–81.CrossRefGoogle Scholar
  8. 8.
    Brenner S . The genetics of Caenorhabditis elegans. Genetics 1974;77:71–94.PubMedGoogle Scholar
  9. 9.
    Ward S, Carrel JS. Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 1979;73:304–21.PubMedCrossRefGoogle Scholar
  10. 10.
    Roberts TM, Stewart M. Nematode sperm locomotion. Curr Opin Cell Biol 1995;7:13–17.PubMedCrossRefGoogle Scholar
  11. 11.
    Ward S . The asymmetric localization of gene products during the development of Caenorhabditis elegans spermatozoa. In: Gall J, ed. Gametogenesis and the early embryo. New York: Alan R. Liss, 1986:55–75.Google Scholar
  12. 12.
    Roberts TM, Pavalko FM, Ward S. Membrane and cytoplasmic proteins are transported in the same organelle complex during nematode spermatogenesis. J Cell Biol 1986;102:1787–96.PubMedCrossRefGoogle Scholar
  13. 13.
    Machaca K, DeFelice LJ, L’Hernault SW. A novel chloride channel localizes to Caenorhabditis elegans spermatids and chloride channel blockers induce spermatid differentiation. Dev Biol 1996;176:1–16.PubMedCrossRefGoogle Scholar
  14. 14.
    L’Hernault SW, Arduengo PM. Mutation of a putative sperm membrane protein in Caenorhabditis elegans prevents sperm differentiation but not its associated meiotic divisions. J Cell Biol 1992;119:55–68.PubMedCrossRefGoogle Scholar
  15. 15.
    Arduengo PM, Appleberry OK, Chuang P, L’Hernault SW. The presenilin protein family member SPE-4 localizes to an ER/Golgi derived organelle and is required for proper cytoplasmic partitioning during Caenorhabditis elegans spermatogenesis. J Cell Sci 1998;111:3645–54.PubMedGoogle Scholar
  16. 16.
    Hardy J . Amyloid, the presenilins and Alzheimer’s disease. Trends Neurosci 1997;20:154–59.PubMedCrossRefGoogle Scholar
  17. 17.
    Shen J, Bronson RT, Chen DF, Xia W, Selkoe DJ, Tonegawa S. Skeletal and CNS defects in presenilin-1-deficient mice. Cell 1997;89:629–39.PubMedCrossRefGoogle Scholar
  18. 18.
    Wong PC, Zheng H, Chen H, et al. Presenilin 1 is required for Notchl and Dll1 expression in the paraxial mesoderm. Nature 1997;387:288–92.PubMedCrossRefGoogle Scholar
  19. 19.
    L’Hernault SW, Shakes DC, Ward S. Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Genetics 1988;120:435–52.PubMedGoogle Scholar
  20. 20.
    Machaca K, L’Hernault SW. The Caenorhabditis elegans spe-5 gene is required for morphogenesis of a sperm-specific organelle and is associated with an inherent cold-sensitive phenotype. Genetics 1997;146:567–81.PubMedGoogle Scholar
  21. 21.
    Ikawa M, Wada I, Kominami K, et al. The putative chaperone calmegin is required for sperm fertility. Nature 1997;387:607–11.PubMedCrossRefGoogle Scholar
  22. 22.
    Singson A, Mercer KB, L’Hernault SW. The C. elegans spe-9 gene encodes a sperm transmembrane protein that contains EGF-like repeats and is required for fertilization. Cell 1998;93:71–79.PubMedCrossRefGoogle Scholar
  23. 23.
    Nelson GA, Ward S. Vesicle fusion, pseudopod extension and amoeboid motility are induced in nematode spermatids by the ionophore monensin. Cell 1980; 19: 457–64.PubMedCrossRefGoogle Scholar
  24. 24.
    Ward S, Hogan E, Nelson GA. The initiation of spermiogenesis in the nematode Caenorhabditis elegans. Dev Biol 1983;98:70–79.PubMedCrossRefGoogle Scholar
  25. 25.
    LaMunyon CW, Ward S. Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proc R Soc Lond B Biol Sci 1998;265:1997–2002.CrossRefGoogle Scholar
  26. 26.
    Singson A, Hill KL, L’Hernault SW. Sperm competition in the absence of fertilization in Caenorhabditis elegans. Genetics 1999;152:201–8.PubMedGoogle Scholar
  27. 27.
    Campbell ID, Bork P. Epidermal growth factor-like modules. Curr Opin Struct Biol 1993;3:385–92.CrossRefGoogle Scholar
  28. 28.
    Weinmaster G . The ins and outs of notch signaling. Mol Cell Neurosci 1997; 9:91–102.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag New York, Inc. 2000

Authors and Affiliations

  • Steven W. L’Hernault
  • Andrew W. Singson

There are no affiliations available

Personalised recommendations