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. 1995 Oct;141(2):551–569. doi: 10.1093/genetics/141.2.551

Enhancers of Glp-1, a Gene Required for Cell-Signaling in Caenorhabditis Elegans, Define a Set of Genes Required for Germline Development

L Qiao 1, J L Lissemore 1, P Shu 1, A Smardon 1, M B Gelber 1, E M Maine 1
PMCID: PMC1206755  PMID: 8647392

Abstract

The distal tip cell (DTC) regulates the proliferation or differentiation choice in the Caenorhabditis elegans germline by an inductive mechanism. Cell signaling requires a putative receptor in the germline, encoded by the glp-1 gene, and a putative signal from the DTC, encoded by the lag-2 gene. Both glp-1 and lag-2 belong to multigene gene families whose members are essential for cell signaling during development of various tissues in insects and vertebrates as well as C. elegans. Relatively little is known about how these pathways regulate cell fate choice. To identify additional genes involved in the glp-1 signaling pathway, we carried out screens for genetic enhancers of glp-1. We recovered mutations in five new genes, named ego (enhancer of glp-1), and two previously identified genes, lag-1 and glp-4, that strongly enhance a weak glp-1 loss-of-function phenotype in the germline. Ego mutations cause multiple phenotypes consistent with the idea that gene activity is required for more than one aspect of germline and, in some cases, somatic development. Based on genetic experiments, glp-1 appears to act upstream of ego-1 and ego-3. We discuss the possible functional relationships among these genes in light of their phenotypes and interactions with glp-1.

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Selected References

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  1. 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]
  2. 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]
  3. 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]
  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. 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]
  6. 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]
  7. Fortini M. E., Artavanis-Tsakonas S. Notch: neurogenesis is only part of the picture. Cell. 1993 Dec 31;75(7):1245–1247. doi: 10.1016/0092-8674(93)90611-s. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Greenwald I. S., Sternberg P. W., Horvitz H. R. The lin-12 locus specifies cell fates in Caenorhabditis elegans. Cell. 1983 Sep;34(2):435–444. doi: 10.1016/0092-8674(83)90377-x. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Honigberg S. M., Conicella C., Espositio R. E. Commitment to meiosis in Saccharomyces cerevisiae: involvement of the SPO14 gene. Genetics. 1992 Apr;130(4):703–716. doi: 10.1093/genetics/130.4.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Honigberg S. M., Esposito R. E. Reversal of cell determination in yeast meiosis: postcommitment arrest allows return to mitotic growth. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6559–6563. doi: 10.1073/pnas.91.14.6559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Horvitz H. R., Brenner S., Hodgkin J., Herman R. K. A uniform genetic nomenclature for the nematode Caenorhabditis elegans. Mol Gen Genet. 1979 Sep;175(2):129–133. doi: 10.1007/BF00425528. [DOI] [PubMed] [Google Scholar]
  14. Hutter H., Schnabel R. glp-1 and inductions establishing embryonic axes in C. elegans. Development. 1994 Jul;120(7):2051–2064. doi: 10.1242/dev.120.7.2051. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Kodoyianni V., Maine E. M., Kimble J. Molecular basis of loss-of-function mutations in the glp-1 gene of Caenorhabditis elegans. Mol Biol Cell. 1992 Nov;3(11):1199–1213. doi: 10.1091/mbc.3.11.1199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Maine E. M., Kimble J. Identification of genes that interact with glp-1, a gene required for inductive cell interactions in Caenorhabditis elegans. Development. 1989 May;106(1):133–143. doi: 10.1242/dev.106.1.133. [DOI] [PubMed] [Google Scholar]
  19. Maine E. M., Kimble J. Suppressors of glp-1, a gene required for cell communication during development in Caenorhabditis elegans, define a set of interacting genes. Genetics. 1993 Dec;135(4):1011–1022. doi: 10.1093/genetics/135.4.1011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Maine E. M., Lissemore J. L., Starmer W. T. A phylogenetic analysis of vertebrate and invertebrate Notch-related genes. Mol Phylogenet Evol. 1995 Jun;4(2):139–149. doi: 10.1006/mpev.1995.1014. [DOI] [PubMed] [Google Scholar]
  21. Mango S. E., Thorpe C. J., Martin P. R., Chamberlain S. H., Bowerman B. Two maternal genes, apx-1 and pie-1, are required to distinguish the fates of equivalent blastomeres in the early Caenorhabditis elegans embryo. Development. 1994 Aug;120(8):2305–2315. doi: 10.1242/dev.120.8.2305. [DOI] [PubMed] [Google Scholar]
  22. Mello C. C., Draper B. W., Priess J. R. The maternal genes apx-1 and glp-1 and establishment of dorsal-ventral polarity in the early C. elegans embryo. Cell. 1994 Apr 8;77(1):95–106. doi: 10.1016/0092-8674(94)90238-0. [DOI] [PubMed] [Google Scholar]
  23. Moskowitz I. P., Gendreau S. B., Rothman J. H. Combinatorial specification of blastomere identity by glp-1-dependent cellular interactions in the nematode Caenorhabditis elegans. Development. 1994 Nov;120(11):3325–3338. doi: 10.1242/dev.120.11.3325. [DOI] [PubMed] [Google Scholar]
  24. Priess J. R. Establishment of initial asymmetry in early Caenorhabditis elegans embryos. Curr Opin Genet Dev. 1994 Aug;4(4):563–568. doi: 10.1016/0959-437x(94)90073-c. [DOI] [PubMed] [Google Scholar]
  25. Priess J. R., Schnabel H., Schnabel R. The glp-1 locus and cellular interactions in early C. elegans embryos. Cell. 1987 Nov 20;51(4):601–611. doi: 10.1016/0092-8674(87)90129-2. [DOI] [PubMed] [Google Scholar]
  26. Schedl T., Graham P. L., Barton M. K., Kimble J. Analysis of the role of tra-1 in germline sex determination in the nematode Caenorhabditis elegans. Genetics. 1989 Dec;123(4):755–769. doi: 10.1093/genetics/123.4.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Seydoux G., Schedl T., Greenwald I. Cell-cell interactions prevent a potential inductive interaction between soma and germline in C. elegans. Cell. 1990 Jun 15;61(6):939–951. doi: 10.1016/0092-8674(90)90060-r. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Sundaram M., Greenwald I. Suppressors of a lin-12 hypomorph define genes that interact with both lin-12 and glp-1 in Caenorhabditis elegans. Genetics. 1993 Nov;135(3):765–783. doi: 10.1093/genetics/135.3.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Wilkinson H. A., Fitzgerald K., Greenwald I. Reciprocal changes in expression of the receptor lin-12 and its ligand lag-2 prior to commitment in a C. elegans cell fate decision. Cell. 1994 Dec 30;79(7):1187–1198. doi: 10.1016/0092-8674(94)90010-8. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Zetka M. C., Rose A. M. The meiotic behavior of an inversion in Caenorhabditis elegans. Genetics. 1992 Jun;131(2):321–332. doi: 10.1093/genetics/131.2.321. [DOI] [PMC free article] [PubMed] [Google Scholar]

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