Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1990 Jun;125(2):351–369. doi: 10.1093/genetics/125.2.351

Dominant Maternal-Effect Mutations Causing Embryonic Lethality in Caenorhabditis Elegans

P E Mains 1, I A Sulston 1, W B Wood 1
PMCID: PMC1204025  PMID: 2379819

Abstract

We undertook screens for dominant, temperature-sensitive, maternal-effect embryonic-lethal mutations of Caenorhabditis elegans as a way to identify certain classes of genes with early embryonic functions, in particular those that are members of multigene families and those that are required in two copies for normal development. The screens have identified eight mutations, representing six loci. Mutations at three of the loci result in only maternal effects on embryonic viability. Mutations at the remaining three loci cause additional nonmaternal (zygotic) effects, including recessive lethality or sterility and dominant male mating defects. Mutations at five of the loci cause visible pregastrulation defects. Three mutations appear to be allelic with a recessive mutation of let-354. Gene dosage experiments indicate that one mutation may be a loss-of-function allele at a haploin sufficient locus. The other mutations appear to result in gain-of-function ``poison'' gene products. Most of these become less deleterious as the relative dosage of the corresponding wild-type allele is increased; we show that relative self-progeny viabilities for the relevant hermaphrodite genotypes are generally M/+/+ > M/+ > M/M/+ > M/Df > M/M, where M represents the dominant mutant allele.

Full Text

The Full Text of this article is available as a PDF (5.3 MB).

Selected References

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

  1. Albers K., Fuchs E. The expression of mutant epidermal keratin cDNAs transfected in simple epithelial and squamous cell carcinoma lines. J Cell Biol. 1987 Aug;105(2):791–806. doi: 10.1083/jcb.105.2.791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Albertson D. G. Formation of the first cleavage spindle in nematode embryos. Dev Biol. 1984 Jan;101(1):61–72. doi: 10.1016/0012-1606(84)90117-9. [DOI] [PubMed] [Google Scholar]
  3. Anderson P., Brenner S. A selection for myosin heavy chain mutants in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4470–4474. doi: 10.1073/pnas.81.14.4470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Bejsovec A., Anderson P. Myosin heavy-chain mutations that disrupt Caenorhabditis elegans thick filament assembly. Genes Dev. 1988 Oct;2(10):1307–1317. doi: 10.1101/gad.2.10.1307. [DOI] [PubMed] [Google Scholar]
  6. Birchler J. A. The genetic basis of dosage compensation of alcohol dehydrogenase-1 in maize. Genetics. 1981 Mar;97(3-4):625–637. doi: 10.1093/genetics/97.3-4.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Cassada R., Isnenghi E., Culotti M., von Ehrenstein G. Genetic analysis of temperature-sensitive embryogenesis mutants in Caenorhabditis elegans. Dev Biol. 1981 May;84(1):193–205. doi: 10.1016/0012-1606(81)90383-3. [DOI] [PubMed] [Google Scholar]
  9. Denell R. E. Homoeosis in Drosophila. II. a Genetic Analysis of Polycomb. Genetics. 1978 Oct;90(2):277–289. doi: 10.1093/genetics/90.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Deppe U., Schierenberg E., Cole T., Krieg C., Schmitt D., Yoder B., von Ehrenstein G. Cell lineages of the embryo of the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1978 Jan;75(1):376–380. doi: 10.1073/pnas.75.1.376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Devlin R. H., Holm D. G., Grigliatti T. A. The influence of whole-arm trisomy on gene expression in Drosophila. Genetics. 1988 Jan;118(1):87–101. doi: 10.1093/genetics/118.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dove W. F. Molecular genetics of Mus musculus: point mutagenesis and millimorgans. Genetics. 1987 May;116(1):5–8. doi: 10.1093/genetics/116.1.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Driever W., Nüsslein-Volhard C. The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell. 1988 Jul 1;54(1):95–104. doi: 10.1016/0092-8674(88)90183-3. [DOI] [PubMed] [Google Scholar]
  14. Edgar L. G., McGhee J. D. Embryonic expression of a gut-specific esterase in Caenorhabditis elegans. Dev Biol. 1986 Mar;114(1):109–118. doi: 10.1016/0012-1606(86)90387-8. [DOI] [PubMed] [Google Scholar]
  15. Gelbart W. M., Irish V. F., St Johnston R. D., Hoffmann F. M., Blackman R. K., Segal D., Posakony L. M., Grimaila R. The decapentaplegic gene complex in Drosophila melanogaster. Cold Spring Harb Symp Quant Biol. 1985;50:119–125. [PubMed] [Google Scholar]
  16. Gergen J. P., Wieschaus E. Dosage requirements for runt in the segmentation of Drosophila embryos. Cell. 1986 Apr 25;45(2):289–299. doi: 10.1016/0092-8674(86)90393-4. [DOI] [PubMed] [Google Scholar]
  17. Goebl M. G., Petes T. D. Most of the yeast genomic sequences are not essential for cell growth and division. Cell. 1986 Sep 26;46(7):983–992. doi: 10.1016/0092-8674(86)90697-5. [DOI] [PubMed] [Google Scholar]
  18. Greenwald I. S., Horvitz H. R. unc-93(e1500): A behavioral mutant of Caenorhabditis elegans that defines a gene with a wild-type null phenotype. Genetics. 1980 Sep;96(1):147–164. doi: 10.1093/genetics/96.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Herskowitz I. Functional inactivation of genes by dominant negative mutations. Nature. 1987 Sep 17;329(6136):219–222. doi: 10.1038/329219a0. [DOI] [PubMed] [Google Scholar]
  20. Hirsh D., Vanderslice R. Temperature-sensitive developmental mutants of Caenorhabditis elegans. Dev Biol. 1976 Mar;49(1):220–235. doi: 10.1016/0012-1606(76)90268-2. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Homyk T., Jr, Emerson C. P., Jr Functional interactions between unlinked muscle genes within haploinsufficient regions of the Drosophila genome. Genetics. 1988 May;119(1):105–121. doi: 10.1093/genetics/119.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Isnenghi E., Cassada R., Smith K., Denich K., Radnia K., von Ehrenstein G. Maternal effects and temperature-sensitive period of mutations affecting embryogenesis in Caenorhabditis elegans. Dev Biol. 1983 Aug;98(2):465–480. doi: 10.1016/0012-1606(83)90376-7. [DOI] [PubMed] [Google Scholar]
  25. Johnsen R. C., Baillie D. L. Formaldehyde mutagenesis of the eT1 balanced region in Caenorhabditis elegans: dose-response curve and the analysis of mutational events. Mutat Res. 1988 Sep;201(1):137–147. doi: 10.1016/0027-5107(88)90120-0. [DOI] [PubMed] [Google Scholar]
  26. Kemphues K. J., Kusch M., Wolf N. Maternal-effect lethal mutations on linkage group II of Caenorhabditis elegans. Genetics. 1988 Dec;120(4):977–986. doi: 10.1093/genetics/120.4.977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kemphues K. J., Priess J. R., Morton D. G., Cheng N. S. Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell. 1988 Feb 12;52(3):311–320. doi: 10.1016/s0092-8674(88)80024-2. [DOI] [PubMed] [Google Scholar]
  28. Kemphues K. J., Raff E. C., Raff R. A., Kaufman T. C. Mutation in a testis-specific beta-tubulin in Drosophila: analysis of its effects on meiosis and map location of the gene. Cell. 1980 Sep;21(2):445–451. doi: 10.1016/0092-8674(80)90481-x. [DOI] [PubMed] [Google Scholar]
  29. Kemphues K. J., Wolf N., Wood W. B., Hirsh D. Two loci required for cytoplasmic organization in early embryos of Caenorhabditis elegans. Dev Biol. 1986 Feb;113(2):449–460. doi: 10.1016/0012-1606(86)90180-6. [DOI] [PubMed] [Google Scholar]
  30. Kramer J. M., Johnson J. J., Edgar R. S., Basch C., Roberts S. The sqt-1 gene of C. elegans encodes a collagen critical for organismal morphogenesis. Cell. 1988 Nov 18;55(4):555–565. doi: 10.1016/0092-8674(88)90214-0. [DOI] [PubMed] [Google Scholar]
  31. Kusch M., Edgar R. S. Genetic studies of unusual loci that affect body shape of the nematode Caenorhabditis elegans and may code for cuticle structural proteins. Genetics. 1986 Jul;113(3):621–639. doi: 10.1093/genetics/113.3.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Laufer J. S., Bazzicalupo P., Wood W. B. Segregation of developmental potential in early embryos of Caenorhabditis elegans. Cell. 1980 Mar;19(3):569–577. doi: 10.1016/s0092-8674(80)80033-x. [DOI] [PubMed] [Google Scholar]
  33. Orkin S. H., Kazazian H. H., Jr The mutation and polymorphism of the human beta-globin gene and its surrounding DNA. Annu Rev Genet. 1984;18:131–171. doi: 10.1146/annurev.ge.18.120184.001023. [DOI] [PubMed] [Google Scholar]
  34. Park E. C., Horvitz H. R. Mutations with dominant effects on the behavior and morphology of the nematode Caenorhabditis elegans. Genetics. 1986 Aug;113(4):821–852. doi: 10.1093/genetics/113.4.821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schedl T., Kimble J. fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics. 1988 May;119(1):43–61. doi: 10.1093/genetics/119.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sigurdson D. C., Herman R. K., Horton C. A., Kari C. K., Pratt S. E. An X-autosome fusion chromosome of Caenorhabditis elegans. Mol Gen Genet. 1986 Feb;202(2):212–218. doi: 10.1007/BF00331639. [DOI] [PubMed] [Google Scholar]
  37. Simpson P. Maternal-Zygotic Gene Interactions during Formation of the Dorsoventral Pattern in Drosophila Embryos. Genetics. 1983 Nov;105(3):615–632. doi: 10.1093/genetics/105.3.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Struhl G. Near-reciprocal phenotypes caused by inactivation or indiscriminate expression of the Drosophila segmentation gene ftz. Nature. 1985 Dec 19;318(6047):677–680. doi: 10.1038/318677a0. [DOI] [PubMed] [Google Scholar]
  39. Waterston R. H. A second informational suppressor, SUP-7 X, in Caenorhabditis elegans. Genetics. 1981 Feb;97(2):307–325. doi: 10.1093/genetics/97.2.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Waterston R. H., Hirsh D., Lane T. R. Dominant mutations affecting muscle structure in Caenorhabditis elegans that map near the actin gene cluster. J Mol Biol. 1984 Dec 15;180(3):473–496. doi: 10.1016/0022-2836(84)90023-8. [DOI] [PubMed] [Google Scholar]
  41. Wood W. B., Hecht R., Carr S., Vanderslice R., Wolf N., Hirsh D. Parental effects and phenotypic characterization of mutations that affect early development in Caenorhabditis elegans. Dev Biol. 1980 Feb;74(2):446–469. doi: 10.1016/0012-1606(80)90445-5. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES