Skip to main content
Genetics logoLink to Genetics
. 1989 Oct;123(2):301–313. doi: 10.1093/genetics/123.2.301

A New Kind of Informational Suppression in the Nematode Caenorhabditis Elegans

J Hodgkin 1, A Papp 1, R Pulak 1, V Ambros 1, P Anderson 1
PMCID: PMC1203802  PMID: 2583479

Abstract

Independent reversions of mutations affecting three different Caenorhabditis elegans genes have each yielded representatives of the same set of extragenic suppressors. Mutations at any one of six loci act as allele-specific recessive suppressors of certain alleles of unc-54 (a myosin heavy chain gene), lin-29 (a heterochronic gene), and tra-2 (a sex determination gene). The same mutations also suppress certain alleles of another sex determination gene, tra-1, and of a morphogenetic gene, dpy-5. In addition to their suppression phenotype, the suppressor mutations cause abnormal morphogenesis of the male bursa and the hermaphrodite vulva. We name these genes smg-1 through smg-6 (suppressor with morphogenetic effect on genitalia), in order to distinguish them from mab (male abnormal) genes that can mutate to produce abnormal genitalia but which do not act as suppressors (smg-1 and smg-2 are new names for two previously described genes, mab-1 and mab-11). The patterns of suppression, and the interactions between the different smg genes, are described and discussed. In general, suppression is recessive and incomplete, and at least some of the suppressed mutations are hypomorphic in nature. A suppressible allele of unc-54 contains a deletion in the 3' noncoding region of the gene; the protein coding region of the gene is apparently unaffected. This suggests that the smg suppressors affect a process other than translation, for example mRNA processing, transport, or stability.

Full Text

The Full Text of this article is available as a PDF (3.4 MB).

Selected References

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

  1. Ambros V., Horvitz H. R. Heterochronic mutants of the nematode Caenorhabditis elegans. Science. 1984 Oct 26;226(4673):409–416. doi: 10.1126/science.6494891. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Cox G. N., Laufer J. S., Kusch M., Edgar R. S. Genetic and Phenotypic Characterization of Roller Mutants of CAENORHABDITIS ELEGANS. Genetics. 1980 Jun;95(2):317–339. doi: 10.1093/genetics/95.2.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dibb N. J., Brown D. M., Karn J., Moerman D. G., Bolten S. L., Waterston R. H. Sequence analysis of mutations that affect the synthesis, assembly and enzymatic activity of the unc-54 myosin heavy chain of Caenorhabditis elegans. J Mol Biol. 1985 Jun 25;183(4):543–551. doi: 10.1016/0022-2836(85)90170-6. [DOI] [PubMed] [Google Scholar]
  5. Doniach T. Activity of the sex-determining gene tra-2 is modulated to allow spermatogenesis in the C. elegans hermaphrodite. Genetics. 1986 Sep;114(1):53–76. doi: 10.1093/genetics/114.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Eggertsson G., Söll D. Transfer ribonucleic acid-mediated suppression of termination codons in Escherichia coli. Microbiol Rev. 1988 Sep;52(3):354–374. doi: 10.1128/mr.52.3.354-374.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eide D., Anderson P. Insertion and excision of Caenorhabditis elegans transposable element Tc1. Mol Cell Biol. 1988 Feb;8(2):737–746. doi: 10.1128/mcb.8.2.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Eide D., Anderson P. The gene structures of spontaneous mutations affecting a Caenorhabditis elegans myosin heavy chain gene. Genetics. 1985 Jan;109(1):67–79. doi: 10.1093/genetics/109.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Epstein H. F., Waterston R. H., Brenner S. A mutant affecting the heavy chain of myosin in Caenorhabditis elegans. J Mol Biol. 1974 Dec 5;90(2):291–300. doi: 10.1016/0022-2836(74)90374-x. [DOI] [PubMed] [Google Scholar]
  10. Greenwald I., Horvitz H. R. A visible allele of the muscle gene sup-10X of C. elegans. Genetics. 1986 May;113(1):63–72. doi: 10.1093/genetics/113.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hartman P. E., Roth J. R. Mechanisms of suppression. Adv Genet. 1973;17:1–105. doi: 10.1016/s0065-2660(08)60170-4. [DOI] [PubMed] [Google Scholar]
  12. Hodgkin J. Male Phenotypes and Mating Efficiency in CAENORHABDITIS ELEGANS. Genetics. 1983 Jan;103(1):43–64. doi: 10.1093/genetics/103.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hodgkin J. More sex-determination mutants of Caenorhabditis elegans. Genetics. 1980 Nov;96(3):649–664. doi: 10.1093/genetics/96.3.649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hodgkin J. Novel nematode amber suppressors. Genetics. 1985 Oct;111(2):287–310. doi: 10.1093/genetics/111.2.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hodgkin J. Sex determination in the nematode C. elegans: analysis of tra-3 suppressors and characterization of fem genes. Genetics. 1986 Sep;114(1):15–52. doi: 10.1093/genetics/114.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Kondo K., Hodgkin J., Waterston R. H. Differential expression of five tRNA(UAGTrp) amber suppressors in Caenorhabditis elegans. Mol Cell Biol. 1988 Sep;8(9):3627–3635. doi: 10.1128/mcb.8.9.3627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kongsuwan K., Yu Q., Vincent A., Frisardi M. C., Rosbash M., Lengyel J. A., Merriam J. A Drosophila Minute gene encodes a ribosomal protein. Nature. 1985 Oct 10;317(6037):555–558. doi: 10.1038/317555a0. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. MacLeod A. R., Karn J., Brenner S. Molecular analysis of the unc-54 myosin heavy-chain gene of Caenorhabditis elegans. Nature. 1981 Jun 4;291(5814):386–390. doi: 10.1038/291386a0. [DOI] [PubMed] [Google Scholar]
  21. Moerman D. G., Plurad S., Waterston R. H., Baillie D. L. Mutations in the unc-54 myosin heavy chain gene of Caenorhabditis elegans that alter contractility but not muscle structure. Cell. 1982 Jul;29(3):773–781. doi: 10.1016/0092-8674(82)90439-1. [DOI] [PubMed] [Google Scholar]
  22. Murgola E. J. tRNA, suppression, and the code. Annu Rev Genet. 1985;19:57–80. doi: 10.1146/annurev.ge.19.120185.000421. [DOI] [PubMed] [Google Scholar]
  23. Parker R., Siliciano P. G., Guthrie C. Recognition of the TACTAAC box during mRNA splicing in yeast involves base pairing to the U2-like snRNA. Cell. 1987 Apr 24;49(2):229–239. doi: 10.1016/0092-8674(87)90564-2. [DOI] [PubMed] [Google Scholar]
  24. Pulak R. A., Anderson P. Structures of spontaneous deletions in Caenorhabditis elegans. Mol Cell Biol. 1988 Sep;8(9):3748–3754. doi: 10.1128/mcb.8.9.3748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rand J. B., Russell R. L. Choline acetyltransferase-deficient mutants of the nematode Caenorhabditis elegans. Genetics. 1984 Feb;106(2):227–248. doi: 10.1093/genetics/106.2.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Riddle D. L., Brenner S. Indirect suppression in Caenorhabditis elegans. Genetics. 1978 Jun;89(2):299–314. doi: 10.1093/genetics/89.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Roth J. R. Frameshift suppression. Cell. 1981 Jun;24(3):601–602. doi: 10.1016/0092-8674(81)90086-6. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Wickens M., Stephenson P. Role of the conserved AAUAAA sequence: four AAUAAA point mutants prevent messenger RNA 3' end formation. Science. 1984 Nov 30;226(4678):1045–1051. doi: 10.1126/science.6208611. [DOI] [PubMed] [Google Scholar]
  30. Wills N., Gesteland R. F., Karn J., Barnett L., Bolten S., Waterston R. H. The genes sup-7 X and sup-5 III of C. elegans suppress amber nonsense mutations via altered transfer RNA. Cell. 1983 Jun;33(2):575–583. doi: 10.1016/0092-8674(83)90438-5. [DOI] [PubMed] [Google Scholar]
  31. von Mende N., Bird D. M., Albert P. S., Riddle D. L. dpy-13: a nematode collagen gene that affects body shape. Cell. 1988 Nov 18;55(4):567–576. doi: 10.1016/0092-8674(88)90215-2. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES