NONDISJUNCTION MUTANTS OF THE NEMATODE CAENORHABDITIS ELEGANS

Jonathan Hodgkin ¹, H. Robert Horvitz ¹, and Sydney Brenner ¹

¹ M.R.C. Laboratory of Molecular Biology, Hills Road, Cambridge, CB2 2QH, England

The frequency of males (5AA; XO) among the self progeny of wild-type Caenorhabditis elegans hermaphrodites (5AA; XX) is about one in 500. Fifteen him (for "high incidence of males") mutations have been identified that increase this frequency by a factor of ten to 150, as a result of increased X-chromosome nondisjunction. The mutations define ten complementation groups, which have been mapped: nine are autosomal, and one sex linked. Most of the mutants are superficially wild type in anatomy and behavior; however, him-4 mutants display gonadal abnormalities, and unc-86 mutants, which have a Him phenotype, exhibit a variety of anatomical and behavioral abnormalities. All the mutants segregate fertile 3X hermaphrodite progeny as well as XO male progeny. Some produce large numbers of inviable zygotes. Mutants in all ten genes produce diplo-X and nullo-X exceptional ova, and in the four strains tested, diplo-X and nullo-X exceptional sperm are produced by 2X "transformed" males. It appears likely that most of the mutants have defects in both gamete lines of the hermaphrodite. XO males of him strains other than him-4 and unc-86 are similar to wild-type males in anatomy and behavior, and all produce equal or almost equal numbers of haplo-X and nullo-X sperm, and no diplo-X sperm. Male fertility is reduced to varying extents in all him mutants. In four of the strains, nondisjunction during oogenesis has been shown to occur at a reductional division, and in three of these strains, abnormalities in recombination have been demonstrated. One mutant also exhibits autosomal nondisjunction, but many of the others probably do not. Therefore, the X chromosome of C. elegans may differ from the autosomes in the mechanisms controlling its meiotic behavior.——3X hermaphrodites are shorter and less fertile than 2X hermaphrodites, and they produce many inviable zygotes among their self progeny: these are probably 4X zygotes. Haplo-X and diplo-X ova are produced in 2:1 ratio by 3X hermaphrodites. him mutations are expressed in these animals, increasing the frequency of self-progeny males and 2X hermaphrodites.

This article has been cited by other articles:

				R. M. Alcazar, R. Lin, and A. Z. Fire Transmission Dynamics of Heritable Silencing Induced by Double-Stranded RNA in Caenorhabditis elegans Genetics, November 1, 2008; 180(3): 1275 - 1288. [Abstract] [Full Text] [PDF]

				J. G. Y. Lim, R. R. W. Stine, and J. L. Yanowitz Domain-Specific Regulation of Recombination in Caenorhabditis elegans in Response to Temperature, Age and Sex Genetics, October 1, 2008; 180(2): 715 - 726. [Abstract] [Full Text] [PDF]

				E. M. Torres, B. R. Williams, and A. Amon Aneuploidy: Cells Losing Their Balance Genetics, June 1, 2008; 179(2): 737 - 746. [Abstract] [Full Text] [PDF]

				J. L. Yanowitz Genome Integrity Is Regulated by the Caenorhabditis elegans Rad51D Homolog rfs-1 Genetics, May 1, 2008; 179(1): 249 - 262. [Abstract] [Full Text] [PDF]

				J. M. Gladden and B. J. Meyer A ONECUT Homeodomain Protein Communicates X Chromosome Dose to Specify Caenorhabditis elegans Sexual Fate by Repressing a Sex Switch Gene Genetics, November 1, 2007; 177(3): 1621 - 1637. [Abstract] [Full Text] [PDF]

				J. M. Gladden, B. Farboud, and B. J. Meyer Revisiting the X:A Signal That Specifies Caenorhabditis elegans Sexual Fate Genetics, November 1, 2007; 177(3): 1639 - 1654. [Abstract] [Full Text] [PDF]

				H. Sun, B. L. Nelms, S. F. Sleiman, H. M. Chamberlin, and W. Hanna-Rose Modulation of Caenorhabditis elegans Transcription Factor Activity by HIM-8 and the Related Zinc-Finger ZIM Proteins Genetics, October 1, 2007; 177(2): 1221 - 1226. [Abstract] [Full Text] [PDF]

				O. Arum and T. E. Johnson Reduced Expression of the Caenorhabditis elegans p53 Ortholog cep-1 Results in Increased Longevity J. Gerontol. A Biol. Sci. Med. Sci., September 1, 2007; 62(9): 951 - 959. [Abstract] [Full Text] [PDF]

				S. Smolikov, A. Eizinger, K. Schild-Prufert, A. Hurlburt, K. McDonald, J. Engebrecht, A. M. Villeneuve, and M. P. Colaiacovo SYP-3 Restricts Synaptonemal Complex Assembly to Bridge Paired Chromosome Axes During Meiosis in Caenorhabditis elegans Genetics, August 1, 2007; 176(4): 2015 - 2025. [Abstract] [Full Text] [PDF]

				J. Boerckel, D. Walker, and S. Ahmed The Caenorhabditis elegans Rad17 Homolog HPR-17 Is Required for Telomere Replication Genetics, May 1, 2007; 176(1): 703 - 709. [Abstract] [Full Text] [PDF]

				M. Tarailo, R. Kitagawa, and A. M. Rose Suppressors of Spindle Checkpoint Defect (such) Mutants Identify New mdf-1/MAD1 Interactors in Caenorhabditis elegans Genetics, April 1, 2007; 175(4): 1665 - 1679. [Abstract] [Full Text] [PDF]

				J. B. Bessler, K. C. Reddy, M. Hayashi, J. Hodgkin, and A. M. Villeneuve A Role for Caenorhabditis elegans Chromatin-Associated Protein HIM-17 in the Proliferation vs. Meiotic Entry Decision Genetics, April 1, 2007; 175(4): 2029 - 2037. [Abstract] [Full Text] [PDF]

				L. R. Garcia, B. LeBoeuf, and P. Koo Diversity in Mating Behavior of Hermaphroditic and Male-Female Caenorhabditis Nematodes Genetics, April 1, 2007; 175(4): 1761 - 1771. [Abstract] [Full Text] [PDF]

				N. M. Amin, K. Hu, D. Pruyne, D. Terzic, A. Bretscher, and J. Liu A Zn-finger/FH2-domain containing protein, FOZI-1, acts redundantly with CeMyoD to specify striated body wall muscle fates in the Caenorhabditis elegans postembryonic mesoderm Development, January 1, 2007; 134(1): 19 - 29. [Abstract] [Full Text] [PDF]

				D. Blanchard, H. Hutter, J. Fleenor, and A. Fire A Differential Cytolocalization Assay for Analysis of Macromolecular Assemblies in the Eukaryotic Cytoplasm Mol. Cell. Proteomics, November 1, 2006; 5(11): 2175 - 2184. [Abstract] [Full Text] [PDF]

				B. P. Gupta, J. Liu, B. J. Hwang, N. Moghal, and P. W. Sternberg sli-3 Negatively Regulates the LET-23/Epidermal Growth Factor Receptor-Mediated Vulval Induction Pathway in Caenorhabditis elegans Genetics, November 1, 2006; 174(3): 1315 - 1326. [Abstract] [Full Text] [PDF]

				J. Harris, M. Lowden, I. Clejan, M. Tzoneva, J. H. Thomas, J. Hodgkin, and S. Ahmed Mutator Phenotype of Caenorhabditis elegans DNA Damage Checkpoint Mutants Genetics, October 1, 2006; 174(2): 601 - 616. [Abstract] [Full Text] [PDF]

				T. Vellai, D. McCulloch, D. Gems, and A. L. Kovacs Effects of Sex and Insulin/Insulin-Like Growth Factor-1 Signaling on Performance in an Associative Learning Paradigm in Caenorhabditis elegans Genetics, September 1, 2006; 174(1): 309 - 316. [Abstract] [Full Text] [PDF]

				S. C. Weeks, C. Benvenuto, and S. K. Reed When males and hermaphrodites coexist: a review of androdioecy in animals Integr. Comp. Biol., August 1, 2006; 46(4): 449 - 464. [Abstract] [Full Text] [PDF]

				M. L. Foehr, A. S. Lindy, R. C. Fairbank, N. M. Amin, M. Xu, J. Yanowitz, A. Z. Fire, and J. Liu An antagonistic role for the C. elegans Schnurri homolog SMA-9 in modulating TGF{beta} signaling during mesodermal patterning Development, August 1, 2006; 133(15): 2887 - 2896. [Abstract] [Full Text] [PDF]

				N. L. Washington and S. Ward FER-1 regulates Ca2+-mediated membrane fusion during C. elegans spermatogenesis J. Cell Sci., June 15, 2006; 119(12): 2552 - 2562. [Abstract] [Full Text] [PDF]

				T. R. Gruninger, D. G. Gualberto, B. LeBoeuf, and L. R. Garcia Integration of Male Mating and Feeding Behaviors in Caenorhabditis elegans J. Neurosci., January 4, 2006; 26(1): 169 - 179. [Abstract] [Full Text] [PDF]

				E. J. Gleason, W. C. Lindsey, T. L. Kroft, A. W. Singson, and S. W. L'Hernault spe-10 Encodes a DHHC-CRD Zinc-Finger Membrane Protein Required for Endoplasmic Reticulum/Golgi Membrane Morphogenesis During Caenorhabditis elegans Spermatogenesis Genetics, January 1, 2006; 172(1): 145 - 158. [Abstract] [Full Text] [PDF]

				F. Couteau and M. Zetka HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans Genes & Dev., November 15, 2005; 19(22): 2744 - 2756. [Abstract] [Full Text] [PDF]

				M. Hammarlund, M. W. Davis, H. Nguyen, D. Dayton, and E. M. Jorgensen Heterozygous Insertions Alter Crossover Distribution but Allow Crossover Interference in Caenorhabditis elegans Genetics, November 1, 2005; 171(3): 1047 - 1056. [Abstract] [Full Text] [PDF]

				Y. Jiang, V. Horner, and J. Liu The HMX homeodomain protein MLS-2 regulates cleavage orientation, cell proliferation and cell fate specification in the C. elegans postembryonic mesoderm Development, September 15, 2005; 132(18): 4119 - 4130. [Abstract] [Full Text] [PDF]

				N. J. D. Gower, D. S. Walker, and H. A. Baylis Inositol 1,4,5-Trisphosphate Signaling Regulates Mating Behavior in Caenorhabditis elegans Males Mol. Biol. Cell, September 1, 2005; 16(9): 3978 - 3986. [Abstract] [Full Text] [PDF]

				K. Sha and A. Fire Imprinting Capacity of Gamete Lineages in Caenorhabditis elegans Genetics, August 1, 2005; 170(4): 1633 - 1652. [Abstract] [Full Text] [PDF]

				G. Dalpe, L. Brown, and J. G. Culotti Vulva morphogenesis involves attraction of plexin 1-expressing primordial vulva cells to semaphorin 1a sequentially expressed at the vulva midline Development, March 15, 2005; 132(6): 1387 - 1400. [Abstract] [Full Text] [PDF]

				M. Haber, M. Schungel, A. Putz, S. Muller, B. Hasert, and H. Schulenburg Evolutionary History of Caenorhabditis elegans Inferred from Microsatellites: Evidence for Spatial and Temporal Genetic Differentiation and the Occurrence of Outbreeding Mol. Biol. Evol., January 1, 2005; 22(1): 160 - 173. [Abstract] [Full Text] [PDF]

				K. Nabeshima, A. M. Villeneuve, and K. J. Hillers Chromosome-Wide Regulation of Meiotic Crossover Formation in Caenorhabditis elegans Requires Properly Assembled Chromosome Axes Genetics, November 1, 2004; 168(3): 1275 - 1292. [Abstract] [Full Text] [PDF]

				C. Wicky, A. Alpi, M. Passannante, A. Rose, A. Gartner, and F. Muller Multiple Genetic Pathways Involving the Caenorhabditis elegans Bloom's Syndrome Genes him-6, rad-51, and top-3 Are Needed To Maintain Genome Stability in the Germ Line Mol. Cell. Biol., June 1, 2004; 24(11): 5016 - 5027. [Abstract] [Full Text] [PDF]

				G. Dalpe, L. W. Zhang, H. Zheng, and J. G. Culotti Conversion of cell movement responses to Semaphorin-1 and Plexin-1 from attraction to repulsion by lowered levels of specific RAC GTPases in C. elegans Development, May 1, 2004; 131(9): 2073 - 2088. [Abstract] [Full Text] [PDF]

				K. E. Koehler, E. A. Millie, J. P. Cherry, S. E. Schrump, and T. J. Hassold Meiotic Exchange and Segregation in Female Mice Heterozygous for Paracentric Inversions Genetics, March 1, 2004; 166(3): 1199 - 1214. [Abstract] [Full Text] [PDF]

				V. Reinke, I. S. Gil, S. Ward, and K. Kazmer Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans Development, January 15, 2004; 131(2): 311 - 323. [Abstract] [Full Text] [PDF]

				J. Nance, E. M. Munro, and J. R. Priess C. elegans PAR-3 and PAR-6 are required for apicobasal asymmetries associated with cell adhesion and gastrulation Development, November 15, 2003; 130(22): 5339 - 5350. [Abstract] [Full Text] [PDF]

				H. Yu, R. F. Pretot, T. R. Burglin, and P. W. Sternberg Distinct roles of transcription factors EGL-46 and DAF-19 in specifying the functionality of a polycystin-expressing sensory neuron necessary for C. elegans male vulva location behavior Development, November 1, 2003; 130(21): 5217 - 5227. [Abstract] [Full Text] [PDF]

				N. Moghal, L. R. Garcia, L. A. Khan, K. Iwasaki, and P. W. Sternberg Modulation of EGF receptor-mediated vulva development by the heterotrimeric G-protein G{alpha}q and excitable cells in C. elegans Development, October 1, 2003; 130(19): 4553 - 4566. [Abstract] [Full Text] [PDF]

				G.-d. Zhu and S. W. L'Hernault The Caenorhabditis elegans spe-39 Gene Is Required for Intracellular Membrane Reorganization During Spermatogenesis Genetics, September 1, 2003; 165(1): 145 - 157. [Abstract] [Full Text] [PDF]

				B. Zhao, P. Khare, L. Feldman, and J. A. Dent Reversal Frequency in Caenorhabditis elegans Represents an Integrated Response to the State of the Animal and Its Environment J. Neurosci., June 15, 2003; 23(12): 5319 - 5328. [Abstract] [Full Text] [PDF]

				D. C. Shakes, P. L. Sadler, J. M. Schumacher, M. Abdolrasulnia, and A. Golden Developmental defects observed in hypomorphic anaphase-promoting complex mutants are linked to cell cycle abnormalities Development, April 15, 2003; 130(8): 1605 - 1620. [Abstract] [Full Text] [PDF]

				L. R. Garcia and P. W. Sternberg Caenorhabditis elegans UNC-103 ERG-Like Potassium Channel Regulates Contractile Behaviors of Sex Muscles in Males before and during Mating J. Neurosci., April 1, 2003; 23(7): 2696 - 2705. [Abstract] [Full Text] [PDF]

				X. Zhao, Y. Yang, D. H. A. Fitch, and M. A. Herman TLP-1 is an asymmetric cell fate determinant that responds to Wnt signals and controls male tail tip morphogenesis in C. elegans Development, March 5, 2003; 129(6): 1497 - 1508. [Abstract] [Full Text] [PDF]

				A. Garofalo, M.-C. Rowlinson, N. A. Amambua, J. M. Hughes, S. M. Kelly, N. C. Price, A. Cooper, D. G. Watson, M. W. Kennedy, and J. E. Bradley The FAR Protein Family of the Nematode Caenorhabditis elegans. DIFFERENTIAL LIPID BINDING PROPERTIES, STRUCTURAL CHARACTERISTICS, AND DEVELOPMENTAL REGULATION J. Biol. Chem., February 28, 2003; 278(10): 8065 - 8074. [Abstract] [Full Text] [PDF]

				N. Moghal and P. W. Sternberg A component of the transcriptional mediator complex inhibits RAS-dependent vulval fate specification in C. elegans Development, January 1, 2003; 130(1): 57 - 69. [Abstract] [Full Text] [PDF]

				A. S.-R. Pepper, D. J. Killian, and E. J. A. Hubbard Genetic Analysis of Caenorhabditis elegans glp-1 Mutants Suggests Receptor Interaction or Competition Genetics, January 1, 2003; 163(1): 115 - 132. [Abstract] [Full Text] [PDF]

				P. M. Meneely, A. F. Farago, and T. M. Kauffman Crossover Distribution and High Interference for Both the X Chromosome and an Autosome During Oogenesis and Spermatogenesis in Caenorhabditis elegans Genetics, November 1, 2002; 162(3): 1169 - 1177. [Abstract] [Full Text] [PDF]

				R. Lints and S. W. Emmons Regulation of sex-specific differentiation and mating behavior in C. elegans by a new member of the DM domain transcription factor family Genes & Dev., September 15, 2002; 16(18): 2390 - 2402. [Abstract] [Full Text] [PDF]

				A. J. MacQueen, M. P. Colaiacovo, K. McDonald, and A. M. Villeneuve Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans Genes & Dev., September 15, 2002; 16(18): 2428 - 2442. [Abstract] [Full Text] [PDF]

				M. P. Colaiacovo, G. M. Stanfield, K. C. Reddy, V. Reinke, S. K. Kim, and A. M. Villeneuve A Targeted RNAi Screen for Genes Involved in Chromosome Morphogenesis and Nuclear Organization in the Caenorhabditis elegans Germline Genetics, September 1, 2002; 162(1): 113 - 128. [Abstract] [Full Text] [PDF]

				J. Nystrom, Z.-Z. Shen, M. Aili, A. J. Flemming, A. Leroi, and S. Tuck Increased or Decreased Levels of Caenorhabditis elegans lon-3, a Gene Encoding a Collagen, Cause Reciprocal Changes in Body Length Genetics, May 1, 2002; 161(1): 83 - 97. [Abstract] [Full Text] [PDF]

				E. Rogers, J. D. Bishop, J. A. Waddle, J. M. Schumacher, and R. Lin The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis J. Cell Biol., April 15, 2002; 157(2): 219 - 229. [Abstract] [Full Text] [PDF]

				K. Kuno, C. Baba, A. Asaka, C. Matsushima, K. Matsushima, and R. Hosono The Caenorhabditis elegans ADAMTS Family Gene adt-1 Is Necessary for Morphogenesis of the Male Copulatory Organs J. Biol. Chem., March 29, 2002; 277(14): 12228 - 12236. [Abstract] [Full Text] [PDF]

				J. R. Chasnov and K. L. Chow Why Are There Males in the Hermaphroditic Species Caenorhabditis elegans? Genetics, March 1, 2002; 160(3): 983 - 994. [Abstract] [Full Text] [PDF]

				C. Rinaldo, P. Bazzicalupo, S. Ederle, M. Hilliard, and A. La Volpe Roles for Caenorhabditis elegans rad-51 in Meiosis and in Resistance to Ionizing Radiation During Development Genetics, February 1, 2002; 160(2): 471 - 479. [Abstract] [Full Text] [PDF]

				J. Gao, L. Estrada, S. Cho, R. E. Ellis, and J. L. Gorski The Caenorhabditis elegans homolog of FGD1, the human Cdc42 GEF gene responsible for faciogenital dysplasia, is critical for excretory cell morphogenesis Hum. Mol. Genet., December 1, 2001; 10(26): 3049 - 3062. [Abstract] [Full Text] [PDF]

				A. J. MacQueen and A. M. Villeneuve Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2 Genes & Dev., July 1, 2001; 15(13): 1674 - 1687. [Abstract] [Full Text] [PDF]

				A. F. Dernburg Here, There, and Everywhere: Kinetochore Function on Holocentric Chromosomes J. Cell Biol., June 11, 2001; 153(6): F33 - F38. [Abstract] [Full Text] [PDF]

				M. Howe, K. L. McDonald, D. G. Albertson, and B. J. Meyer HIM-10 Is Required for Kinetochore Structure and Function on Caenorhabditis elegans Holocentric Chromosomes J. Cell Biol., June 11, 2001; 153(6): 1227 - 1238. [Abstract] [Full Text] [PDF]

				A. Sugimoto, A. Kusano, R. R. Hozak, W. B. Derry, J. Zhu, and J. H. Rothman Many Genomic Regions Are Required for Normal Embryonic Programmed Cell Death in Caenorhabditis elegans Genetics, May 1, 2001; 158(1): 237 - 252. [Abstract] [Full Text]

				G. M. Chin and A. M. Villeneuve C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G2 DNA damage checkpoint Genes & Dev., March 1, 2001; 15(5): 522 - 534. [Abstract] [Full Text]

I. Oishi, K. Iwai, Y. Kagohashi, H. Fujimoto, K.-I. Kariya, T. Kataoka, H. Sawa, H. Okano, H. Otani, H. Yamamura, et al. Critical Role of Caenorhabditis elegans Homologs of Cds1 (Chk2)-Related Kinases in Meiotic Recombination Mol. Cell. Biol., February 15, 2001; 21(4): 1329 - 1335.