Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1997 Jan;145(1):111–121. doi: 10.1093/genetics/145.1.111

Glp-3 Is Required for Mitosis and Meiosis in the Caenorhabditis Elegans Germ Line

L C Kadyk 1, E J Lambie 1, J Kimble 1
PMCID: PMC1207770  PMID: 9017394

Abstract

The germ line is the only tissue in Caenorhabditis elegans in which a stem cell population continues to divide mitotically throughout life; hence the cell cycles of the germ line and the soma are regulated differently. Here we report the genetic and phenotypic characterization of the glp-3 gene. In animals homozygous for each of five recessive loss-of-function alleles, germ cells in both hermaphrodites and males fail to progress through mitosis and meiosis, but somatic cells appear to divide normally. Germ cells in animals grown at 15° appear by DAPI staining to be uniformly arrested at the G2/M transition with <20 germ cells per gonad on average, suggesting a checkpoint-mediated arrest. In contrast, germ cells in mutant animals grown at 25° frequently proliferate slowly during adulthood, eventually forming small germ lines with several hundred germ cells. Nevertheless, cells in these small germ lines never undergo meiosis. Double mutant analysis with mutations in other genes affecting germ cell proliferation supports the idea that glp-3 may encode a gene product that is required for the mitotic and meiotic cell cycles in the C. elegans germ line.

Full Text

The Full Text of this article is available as a PDF (3.0 MB).

Selected References

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

  1. Alphey L., Jimenez J., White-Cooper H., Dawson I., Nurse P., Glover D. M. twine, a cdc25 homolog that functions in the male and female germline of Drosophila. Cell. 1992 Jun 12;69(6):977–988. doi: 10.1016/0092-8674(92)90616-k. [DOI] [PubMed] [Google Scholar]
  2. Aroian R. V., Sternberg P. W. Multiple functions of let-23, a Caenorhabditis elegans receptor tyrosine kinase gene required for vulval induction. Genetics. 1991 Jun;128(2):251–267. doi: 10.1093/genetics/128.2.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Artavanis-Tsakonas S., Matsuno K., Fortini M. E. Notch signaling. Science. 1995 Apr 14;268(5208):225–232. doi: 10.1126/science.7716513. [DOI] [PubMed] [Google Scholar]
  4. Austin J., Kimble J. Transcript analysis of glp-1 and lin-12, homologous genes required for cell interactions during development of C. elegans. Cell. 1989 Aug 11;58(3):565–571. doi: 10.1016/0092-8674(89)90437-6. [DOI] [PubMed] [Google Scholar]
  5. Austin J., Kimble J. glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell. 1987 Nov 20;51(4):589–599. doi: 10.1016/0092-8674(87)90128-0. [DOI] [PubMed] [Google Scholar]
  6. Barton M. K., Kimble J. fog-1, a regulatory gene required for specification of spermatogenesis in the germ line of Caenorhabditis elegans. Genetics. 1990 May;125(1):29–39. doi: 10.1093/genetics/125.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Beanan M. J., Strome S. Characterization of a germ-line proliferation mutation in C. elegans. Development. 1992 Nov;116(3):755–766. doi: 10.1242/dev.116.3.755. [DOI] [PubMed] [Google Scholar]
  9. Christensen S., Kodoyianni V., Bosenberg M., Friedman L., Kimble J. lag-1, a gene required for lin-12 and glp-1 signaling in Caenorhabditis elegans, is homologous to human CBF1 and Drosophila Su(H). Development. 1996 May;122(5):1373–1383. doi: 10.1242/dev.122.5.1373. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Crittenden S. L., Troemel E. R., Evans T. C., Kimble J. GLP-1 is localized to the mitotic region of the C. elegans germ line. Development. 1994 Oct;120(10):2901–2911. doi: 10.1242/dev.120.10.2901. [DOI] [PubMed] [Google Scholar]
  12. Edgar B. A., O'Farrell P. H. The three postblastoderm cell cycles of Drosophila embryogenesis are regulated in G2 by string. Cell. 1990 Aug 10;62(3):469–480. doi: 10.1016/0092-8674(90)90012-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Francis R., Barton M. K., Kimble J., Schedl T. gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics. 1995 Feb;139(2):579–606. doi: 10.1093/genetics/139.2.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hartwell L. H., Mortimer R. K., Culotti J., Culotti M. Genetic Control of the Cell Division Cycle in Yeast: V. Genetic Analysis of cdc Mutants. Genetics. 1973 Jun;74(2):267–286. doi: 10.1093/genetics/74.2.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Henderson S. T., Gao D., Lambie E. J., Kimble J. lag-2 may encode a signaling ligand for the GLP-1 and LIN-12 receptors of C. elegans. Development. 1994 Oct;120(10):2913–2924. doi: 10.1242/dev.120.10.2913. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Kimble J. E., White J. G. On the control of germ cell development in Caenorhabditis elegans. Dev Biol. 1981 Jan 30;81(2):208–219. doi: 10.1016/0012-1606(81)90284-0. [DOI] [PubMed] [Google Scholar]
  18. Lambie E. J., Kimble J. Two homologous regulatory genes, lin-12 and glp-1, have overlapping functions. Development. 1991 May;112(1):231–240. doi: 10.1242/dev.112.1.231. [DOI] [PubMed] [Google Scholar]
  19. Nurse P., Bissett Y. Gene required in G1 for commitment to cell cycle and in G2 for control of mitosis in fission yeast. Nature. 1981 Aug 6;292(5823):558–560. doi: 10.1038/292558a0. [DOI] [PubMed] [Google Scholar]
  20. Piggott J. R., Rai R., Carter B. L. A bifunctional gene product involved in two phases of the yeast cell cycle. Nature. 1982 Jul 22;298(5872):391–393. doi: 10.1038/298391a0. [DOI] [PubMed] [Google Scholar]
  21. Qiao L., Lissemore J. L., Shu P., Smardon A., Gelber M. B., Maine E. M. Enhancers of glp-1, a gene required for cell-signaling in Caenorhabditis elegans, define a set of genes required for germline development. Genetics. 1995 Oct;141(2):551–569. doi: 10.1093/genetics/141.2.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schild D., Byers B. Meiotic effects of DNA-defective cell division cycle mutations of Saccharomyces cerevisiae. Chromosoma. 1978 Dec 21;70(1):109–130. doi: 10.1007/BF00292220. [DOI] [PubMed] [Google Scholar]
  23. Schnabel R. Pattern formation: regional specification in the early C. elegans embryo. Bioessays. 1996 Jul;18(7):591–594. doi: 10.1002/bies.950180711. [DOI] [PubMed] [Google Scholar]
  24. Shuster E. O., Byers B. Pachytene arrest and other meiotic effects of the start mutations in Saccharomyces cerevisiae. Genetics. 1989 Sep;123(1):29–43. doi: 10.1093/genetics/123.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tax F. E., Yeargers J. J., Thomas J. H. Sequence of C. elegans lag-2 reveals a cell-signalling domain shared with Delta and Serrate of Drosophila. Nature. 1994 Mar 10;368(6467):150–154. doi: 10.1038/368150a0. [DOI] [PubMed] [Google Scholar]
  26. Weber L., Byers B. A RAD9-dependent checkpoint blocks meiosis of cdc13 yeast cells. Genetics. 1992 May;131(1):55–63. doi: 10.1093/genetics/131.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Yochem J., Greenwald I. glp-1 and lin-12, genes implicated in distinct cell-cell interactions in C. elegans, encode similar transmembrane proteins. Cell. 1989 Aug 11;58(3):553–563. doi: 10.1016/0092-8674(89)90436-4. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES