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. 2003 Jan;163(1):133–146. doi: 10.1093/genetics/163.1.133

Control of vulval competence and centering in the nematode Oscheius sp. 1 CEW1.

Sophie Louvet-Vallée 1, Irina Kolotuev 1, Benjamin Podbilewicz 1, Marie-Anne Félix 1
PMCID: PMC1462419  PMID: 12586702

Abstract

To compare vulva development mechanisms in the nematode Oscheius sp. 1 to those known in Caenorhabditis elegans, we performed a genetic screen for vulva mutants in Oscheius sp. 1 CEW1. Here we present one large category of mutations that we call cov, which affect the specification of the Pn.p ventral epidermal cells along the antero-posterior axis. The Pn.p cells are numbered from 1 to 12 from anterior to posterior. In wild-type Oscheius sp. 1 CEW1, the P(4-8).p cells are competent to form the vulva and the progeny of P(5-7).p actually form the vulva, with the descendants of P6.p adopting a central vulval fate. Among the 17 mutations (defining 13 genes) that we characterize here, group 1 mutations completely or partially abolish P(4-8).p competence, and this correlates with early fusion of the Pn.p cells to the epidermal syncytium. In this group, we found a putative null mutation in the lin-39 HOM-C homolog, the associated phenotype of which could be weakly mimicked by injection of a morpholino against Osp1-lin-39 in the mother's germ line. Using cell ablation in a partially penetrant competence mutant, we show that vulval competence is partially controlled by a gonadal signal. Most other mutants found in the screen display phenotypes unknown in C. elegans. Group 2 mutants show a partial penetrance of Pn.p competence loss and an abnormal centering of the vulva on P5.p, suggesting that these two processes are coregulated by the same pathway in Oscheius sp. 1. Group 3 mutants display an enlarged competence group that includes P3.p, thus demonstrating the existence of a specific mechanism inhibiting P3.p competence. Group 4 mutants display an abnormal centering of the vulval pattern on P7.p and suggest that a specific mechanism centers the vulval pattern on a single Pn.p cell.

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Selected References

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  1. Ahringer J. Maternal control of a zygotic patterning gene in Caenorhabditis elegans. Development. 1997 Oct;124(19):3865–3869. doi: 10.1242/dev.124.19.3865. [DOI] [PubMed] [Google Scholar]
  2. Alper S., Kenyon C. REF-1, a protein with two bHLH domains, alters the pattern of cell fusion in C. elegans by regulating Hox protein activity. Development. 2001 May;128(10):1793–1804. doi: 10.1242/dev.128.10.1793. [DOI] [PubMed] [Google Scholar]
  3. Alper Scott, Kenyon Cynthia. The zinc finger protein REF-2 functions with the Hox genes to inhibit cell fusion in the ventral epidermis of C. elegans. Development. 2002 Jul;129(14):3335–3348. doi: 10.1242/dev.129.14.3335. [DOI] [PubMed] [Google Scholar]
  4. Clandinin T. R., Katz W. S., Sternberg P. W. Caenorhabditis elegans HOM-C genes regulate the response of vulval precursor cells to inductive signal. Dev Biol. 1997 Feb 1;182(1):150–161. doi: 10.1006/dbio.1996.8471. [DOI] [PubMed] [Google Scholar]
  5. Clark S. G., Chisholm A. D., Horvitz H. R. Control of cell fates in the central body region of C. elegans by the homeobox gene lin-39. Cell. 1993 Jul 16;74(1):43–55. doi: 10.1016/0092-8674(93)90293-y. [DOI] [PubMed] [Google Scholar]
  6. Delattre M., Félix M. A. Development and evolution of a variable left-right asymmetry in nematodes: the handedness of P11/P12 migration. Dev Biol. 2001 Apr 15;232(2):362–371. doi: 10.1006/dbio.2001.0175. [DOI] [PubMed] [Google Scholar]
  7. Delattre M., Félix M. A. Microevolutionary studies in nematodes: a beginning. Bioessays. 2001 Sep;23(9):807–819. doi: 10.1002/bies.1116. [DOI] [PubMed] [Google Scholar]
  8. Delattre M., Félix M. A. Polymorphism and evolution of vulval precursor cell lineages within two nematode genera, Caenorhabditis and Oscheius. Curr Biol. 2001 May 1;11(9):631–643. doi: 10.1016/s0960-9822(01)00202-0. [DOI] [PubMed] [Google Scholar]
  9. Eisenmann D. M., Kim S. K. Protruding vulva mutants identify novel loci and Wnt signaling factors that function during Caenorhabditis elegans vulva development. Genetics. 2000 Nov;156(3):1097–1116. doi: 10.1093/genetics/156.3.1097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eisenmann D. M., Maloof J. N., Simske J. S., Kenyon C., Kim S. K. The beta-catenin homolog BAR-1 and LET-60 Ras coordinately regulate the Hox gene lin-39 during Caenorhabditis elegans vulval development. Development. 1998 Sep;125(18):3667–3680. doi: 10.1242/dev.125.18.3667. [DOI] [PubMed] [Google Scholar]
  11. Eizinger A., Sommer R. J. The homeotic gene lin-39 and the evolution of nematode epidermal cell fates. Science. 1997 Oct 17;278(5337):452–455. doi: 10.1126/science.278.5337.452. [DOI] [PubMed] [Google Scholar]
  12. Ferguson E. L., Horvitz H. R. Identification and characterization of 22 genes that affect the vulval cell lineages of the nematode Caenorhabditis elegans. Genetics. 1985 May;110(1):17–72. doi: 10.1093/genetics/110.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ferguson E. L., Sternberg P. W., Horvitz H. R. A genetic pathway for the specification of the vulval cell lineages of Caenorhabditis elegans. Nature. 1987 Mar 19;326(6110):259–267. doi: 10.1038/326259a0. [DOI] [PubMed] [Google Scholar]
  14. Finney M., Ruvkun G. The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell. 1990 Nov 30;63(5):895–905. doi: 10.1016/0092-8674(90)90493-x. [DOI] [PubMed] [Google Scholar]
  15. Francis R., Waterston R. H. Muscle cell attachment in Caenorhabditis elegans. J Cell Biol. 1991 Aug;114(3):465–479. doi: 10.1083/jcb.114.3.465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Félix M. A., De Ley P., Sommer R. J., Frisse L., Nadler S. A., Thomas W. K., Vanfleteren J., Sternberg P. W. Evolution of vulva development in the Cephalobina (Nematoda). Dev Biol. 2000 May 1;221(1):68–86. doi: 10.1006/dbio.2000.9665. [DOI] [PubMed] [Google Scholar]
  17. Félix M. A., Sternberg P. W. Two nested gonadal inductions of the vulva in nematodes. Development. 1997 Jan;124(1):253–259. doi: 10.1242/dev.124.1.253. [DOI] [PubMed] [Google Scholar]
  18. Grandien K., Sommer R. J. Functional comparison of the nematode Hox gene lin-39 in C. elegans and P. pacificus reveals evolutionary conservation of protein function despite divergence of primary sequences. Genes Dev. 2001 Aug 15;15(16):2161–2172. doi: 10.1101/gad.200601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hoier E. F., Mohler W. A., Kim S. K., Hajnal A. The Caenorhabditis elegans APC-related gene apr-1 is required for epithelial cell migration and Hox gene expression. Genes Dev. 2000 Apr 1;14(7):874–886. [PMC free article] [PubMed] [Google Scholar]
  20. Horvitz H. R., Sternberg P. W. Multiple intercellular signalling systems control the development of the Caenorhabditis elegans vulva. Nature. 1991 Jun 13;351(6327):535–541. doi: 10.1038/351535a0. [DOI] [PubMed] [Google Scholar]
  21. Horvitz H. R., Sulston J. E. Isolation and genetic characterization of cell-lineage mutants of the nematode Caenorhabditis elegans. Genetics. 1980 Oct;96(2):435–454. doi: 10.1093/genetics/96.2.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jungblut B., Sommer R. J. The nematode even-skipped homolog vab-7 regulates gonad and vulva position in Pristionchus pacificus. Development. 2001 Jan;128(2):253–261. doi: 10.1242/dev.128.2.253. [DOI] [PubMed] [Google Scholar]
  23. Kimble J., Hirsh D. The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev Biol. 1979 Jun;70(2):396–417. doi: 10.1016/0012-1606(79)90035-6. [DOI] [PubMed] [Google Scholar]
  24. Maloof J. N., Kenyon C. The Hox gene lin-39 is required during C. elegans vulval induction to select the outcome of Ras signaling. Development. 1998 Jan;125(2):181–190. doi: 10.1242/dev.125.2.181. [DOI] [PubMed] [Google Scholar]
  25. Mohler William A., Shemer Gidi, del Campo Jacob J., Valansi Clari, Opoku-Serebuoh Eugene, Scranton Victoria, Assaf Nirit, White John G., Podbilewicz Benjamin. The type I membrane protein EFF-1 is essential for developmental cell fusion. Dev Cell. 2002 Mar;2(3):355–362. doi: 10.1016/s1534-5807(02)00129-6. [DOI] [PubMed] [Google Scholar]
  26. Podbilewicz B. ADM-1, a protein with metalloprotease- and disintegrin-like domains, is expressed in syncytial organs, sperm, and sheath cells of sensory organs in Caenorhabditis elegans. Mol Biol Cell. 1996 Dec;7(12):1877–1893. doi: 10.1091/mbc.7.12.1877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sharma-Kishore R., White J. G., Southgate E., Podbilewicz B. Formation of the vulva in Caenorhabditis elegans: a paradigm for organogenesis. Development. 1999 Feb;126(4):691–699. doi: 10.1242/dev.126.4.691. [DOI] [PubMed] [Google Scholar]
  28. Shemer G., Kishore R., Podbilewicz B. Ring formation drives invagination of the vulva in Caenorhabditis elegans: Ras, cell fusion, and cell migration determine structural fates. Dev Biol. 2000 May 1;221(1):233–248. doi: 10.1006/dbio.2000.9657. [DOI] [PubMed] [Google Scholar]
  29. Shemer Gidi, Podbilewicz Benjamin. LIN-39/Hox triggers cell division and represses EFF-1/fusogen-dependent vulval cell fusion. Genes Dev. 2002 Dec 15;16(24):3136–3141. doi: 10.1101/gad.251202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sommer R. J., Eizinger A., Lee K. Z., Jungblut B., Bubeck A., Schlak I. The Pristionchus HOX gene Ppa-lin-39 inhibits programmed cell death to specify the vulva equivalence group and is not required during vulval induction. Development. 1998 Oct;125(19):3865–3873. doi: 10.1242/dev.125.19.3865. [DOI] [PubMed] [Google Scholar]
  31. Sommer R. J., Sternberg P. W. Apoptosis and change of competence limit the size of the vulva equivalence group in Pristionchus pacificus: a genetic analysis. Curr Biol. 1996 Jan 1;6(1):52–59. doi: 10.1016/s0960-9822(02)00421-9. [DOI] [PubMed] [Google Scholar]
  32. Sternberg P. W., Horvitz H. R. Pattern formation during vulval development in C. elegans. Cell. 1986 Mar 14;44(5):761–772. doi: 10.1016/0092-8674(86)90842-1. [DOI] [PubMed] [Google Scholar]
  33. Sternberg P. W., Horvitz H. R. Postembryonic nongonadal cell lineages of the nematode Panagrellus redivivus: description and comparison with those of Caenorhabditis elegans. Dev Biol. 1982 Sep;93(1):181–205. doi: 10.1016/0012-1606(82)90251-2. [DOI] [PubMed] [Google Scholar]
  34. Sulston J. E., Horvitz H. R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol. 1977 Mar;56(1):110–156. doi: 10.1016/0012-1606(77)90158-0. [DOI] [PubMed] [Google Scholar]
  35. Trent C., Tsuing N., Horvitz H. R. Egg-laying defective mutants of the nematode Caenorhabditis elegans. Genetics. 1983 Aug;104(4):619–647. doi: 10.1093/genetics/104.4.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wang B. B., Müller-Immergluck M. M., Austin J., Robinson N. T., Chisholm A., Kenyon C. A homeotic gene cluster patterns the anteroposterior body axis of C. elegans. Cell. 1993 Jul 16;74(1):29–42. doi: 10.1016/0092-8674(93)90292-x. [DOI] [PubMed] [Google Scholar]
  37. Wang M., Sternberg P. W. Pattern formation during C. elegans vulval induction. Curr Top Dev Biol. 2001;51:189–220. doi: 10.1016/s0070-2153(01)51006-6. [DOI] [PubMed] [Google Scholar]

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