Embryonic Development in Caenorhabditis elegans

Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 18)


Nematodes were first used to study of embryogenesis more than 100 years ago, and this in part led to the concepts of cell-autonomous differentiation and localized cytoplasmic determinants. More recently, the techniques of genetics, experimental and descriptive embryology, and molecular biology have been combined to study the development of the small, free-living nematode Caenorhabditis elegans (Brenner 1974, 1988). This chapter focuses on embryonic development and is intended as a general overview of C. elegans embryogenesis, illustrating the experimental techniques available for this organism and the conclusions that can be drawn. Excellent reviews on postembryonic development (i.e. after hatching) in C. elegans and most other aspects of the worm’s development, genetics and biology can be found in Wood (1988a). This book includes extensive appendices detailing techniques and anatomy and includes phenotypic descriptions of all mutants known at the time of publication. Other reviews of C. elegans embryogenesis can be found in Kemphues (1989), Wood (1988b), Schierenberg (1989) and Strome (1989).


Cold Spring Harbor Caenorhabditis Elegans Nematode Caenorhabditis Elegans Anchor Cell Founder Cell 
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  1. Aamodt EJ, Chung MA, McGhee JD (1991) Spatial control of gut-specific gene expression during Caenorhabditis elegans development. Science 252: 579–582PubMedCrossRefGoogle Scholar
  2. Albertson DG (1984) Formation of the first cleavage spindle in nematode embryos. Dev Biol 101: 61–72PubMedCrossRefGoogle Scholar
  3. Albertson DG, Thomson JN (1982) The kinetochores of Caenorhabditis elegans. Chromosoma 86: 409–428PubMedCrossRefGoogle Scholar
  4. Anderson P, Brenner S (1984) A selection for myosin heavy-chain mutants in the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 81: 4470–4474PubMedCrossRefGoogle Scholar
  5. Aroian RV, Koga M, Mendel JE, Ohshima Y, Sternberg, P (1991) The let-23 gene necessary for Caenorhabditis elegans vulval induction encodes a tyrosine kinase of the EGF receptor subfamily. Nature (London) 348: 693–699CrossRefGoogle Scholar
  6. Austin J Kimble J (1987) glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in Caenorhabditis elegans. Cell 51:589–599Google Scholar
  7. Austin J, Kimble J (1989) Transcript analysis of glp-1 and lin-12, homologous genes required for cell interactions during development of C. elegans. Cell 58: 565–571PubMedCrossRefGoogle Scholar
  8. Babu P (1974) Biochemical genetics of Caenorhabditis elegans. Mol Gen Genet 135: 39–44CrossRefGoogle Scholar
  9. Beitel GJ, Clark SG, Horvitz, HR (1991) Caenorhabditis elegans ras gene let-60 acts as a switch in the pathway of vulval induction. Nature (London) 348: 503–509Google Scholar
  10. Bennett KL, Ward S (1986) Neither a germ line-specific nor several somatically expressed genes are lost during embryonic chromatin diminution in the nematode Ascaris lumbricoides. Dev Biol 118: 141–147PubMedCrossRefGoogle Scholar
  11. Boveri T (1910) Über die Teilung centrifugierter Eier von Ascaris megalocephala. Wilhelm Roux’s Arch Entwicklungsmech Org 30: 101–125Google Scholar
  12. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94PubMedGoogle Scholar
  13. Brenner S (1988) Forward. In: Wood WB (ed) The nematode Caenorhabditis elegans. Cold Spring Harbor Press, Cold Spring Harbor, New YorkGoogle Scholar
  14. Brenner S, Dove W, Herskowitz I, Thomas R (1990) Genes and development: molecular and logical themes. Genetics 126: 479–486PubMedGoogle Scholar
  15. Carter PW, Roos JM, Kemphues KJ (1990) Molecular analysis of zyg-11, a maternal-effect gene required for early embryogenesis of Caenorhabditis elegans. Mol Gen Genet 221: 72–80PubMedCrossRefGoogle Scholar
  16. Cassada R, Isnenghi E, Culotti M, von Ehrenstein G (1981) Genetic analysis of temperature-sensitive embryogenesis mutants in Caenorhabditis elegans. Dev Biol 84: 193–205PubMedCrossRefGoogle Scholar
  17. Cleavinger PJ, McDowell JW, Bennett KL (1989) Transcription in nematodes: early Ascaris embryos are transcriptionally active. Dev Biol 133: 600–604PubMedCrossRefGoogle Scholar
  18. Collins J, Saari B, Anderson P (1987) Activation of a transposable element in the germ line but not the soma of Caenorhabditis elegans. Nature (London) 328: 726–728CrossRefGoogle Scholar
  19. Coulson A, Sulston J, Brenner S, Kam J (1986) Toward a physical map of the genome of the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 83: 7821–7825PubMedCrossRefGoogle Scholar
  20. Coulson A, Waterston R, Kiff J, Sulston J, Kohara Y (1988) Genome linking with yeast artificial chromosomes. Nature (London) 335: 184–186CrossRefGoogle Scholar
  21. Cowan AE, McIntosh JR (1985) Mapping the distribution of differentiation potential for intestine, muscle, and hypodermis during early development in Caenorhabditis elegans. Cell 41: 923–932PubMedCrossRefGoogle Scholar
  22. Davidson EH (1986) Gene activity in early development. Academic Press, New YorkGoogle Scholar
  23. Davidson EH (1990) How embryos work: a comparative view of diverse modes of cell fate specification. Development 108: 365–389PubMedGoogle Scholar
  24. Denich KTR, Schierenberg E, Isnenghi E, Cassada R (1984) Cell-lineage and developmental defects of temperature-sensitive embryonic arrest mutants of the nematode Caenorhabditis elegans. Wilhelm Roux’s Arch Dev Biol 193: 164179Google Scholar
  25. Deppe U, Schierenberg E, Cole T, Krieg C, Schmitt D, Yoder B, von Ehrenstein G (1978) Cell lineages of the embryo of the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 75: 376–380PubMedCrossRefGoogle Scholar
  26. Dove WF (1987) Molecular genetics of Mus musculus: point mutagenesis and millimorgans. Genetics 116: 6–8Google Scholar
  27. Driever W, Nusslein-Vohard C (1988a) A gradient of biciod protein in Drosophila embryos. Cell 54: 83–93PubMedCrossRefGoogle Scholar
  28. Driever W, Nusslein-Vohard C (1988b) The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54: 95–104PubMedCrossRefGoogle Scholar
  29. Eddy EM (1975) Germ plasm and the differentiation of the germ line. Int Rev Cytol 43: 229–280PubMedCrossRefGoogle Scholar
  30. Edgar LG, McGhee JD (1986) Embryonic expression of a gut-specific esterase in Caenorhabditis elegans. Dev Biol 114: 109–118PubMedCrossRefGoogle Scholar
  31. Edgar LG, McGhee JD (1988) DNA synthesis and the control of embryonic gene expression in Caenorhabditis elegans. Cell 53: 589–599PubMedCrossRefGoogle Scholar
  32. Edgley ML, Riddle DL (1990) The nematode Caenorhabditis elegans. Genetic Maps 5:3. 111–3. 133Google Scholar
  33. Emmons SW (1988) The genome, In: Wood WB (ed) The nematode Caenorhabditis elegans. Cold Spring Harbor Press, Cold Spring Harbor, New YorkGoogle Scholar
  34. Emmons SW, Klass MR, Hirsh D (1979) Analysis of the constancy of DNA sequences during development and evolution of the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 76: 1333–1337PubMedCrossRefGoogle Scholar
  35. Fire A (1986) Integrative transformation of Caenorhabditis elegans. EMBO J 5: 2673–2680PubMedGoogle Scholar
  36. Goebl MG, Petes TD (1986) Most of the yeast genomic sequences are not essential for cell growth and division. Cell 46: 983–992PubMedCrossRefGoogle Scholar
  37. Greenwald I (1985) lin-12,a nematode homeotic gene, is homologous to a set ofGoogle Scholar
  38. mammalian proteins that includes epidermal growth factor. Cell 43:583–590 Han M, Sternberg PW (1991) let-60,a gene that specifies cell fate during C. elegans Google Scholar
  39. vulval induction, encodes a ras protein. Cell 63:921–931Google Scholar
  40. Hecht RM, Gossett LA, Jeffery WR (1981) Ontogeny of maternal and newly transcribed mRNA analyzed by in situ hybridization during development of Caenorhabditis elegans. Dev Biol 83: 374–379PubMedCrossRefGoogle Scholar
  41. Hecht RM, Berg-Zabelshansky M, Rao PN, Davis FM (1987) Conditional absence of mitosis-specific antigens in a temperature-sensitive embryonic arrest mutant of Caenorhabditis elegans. J Cell Sci 87: 305–314PubMedGoogle Scholar
  42. Herman RK (1978) Crossover suppressors and balanced recessive lethal in Caenorhabditis elegans. Genetics 88: 49–65PubMedGoogle Scholar
  43. Herman RK (1988) Genetics. In: Wood WB (ed) The nematode Caenorhabditis elegans. Cold Spring Harbor Press, Cold Spring Harbor, New YorkGoogle Scholar
  44. Herman RK, Hedgecock EM (1990) Limitations of the size of the vulval primordium of Caenorhabditis elegans by lin-15 expression in surrounding hypodermis. Nature (London) 348: 169–171CrossRefGoogle Scholar
  45. Hill DP, Strome S (1988) An analysis of the role of microfilaments in the establishment and maintenance of asymmetry in Caenorhabditis elegans zygotes. Dev Biol 125: 75–84PubMedCrossRefGoogle Scholar
  46. Hill DP, Strome S (1990) Brief cytochalasin-induced disruption of microfilaments during a critical interval in 1-cell C. elegans embryos alters the partitioning of developmental instructions to the 2-cell embryo. Development 108: 159172Google Scholar
  47. Hill DP, Shakes DC, Ward S, Strome S (1989) A sperm-supplied product essential for initiation of normal embryogenesis in Caenorhabditis elegans is encoded by the paternal-effect embryonic-lethal gene, spe-11. Dev Biol 136: 154–166PubMedCrossRefGoogle Scholar
  48. Hirsh D, Vanderslice R (1976) Temperature-sensitive developmental mutants of Caenorhabditis elegans. Dev Biol 49: 220–235PubMedCrossRefGoogle Scholar
  49. Hirsh D, Kemphues KJ, Stinchcomb DT, Jefferson R (1985) Genes affecting early development in Caenorhabditis elegans. Cold Spring Harbor Symp Quant Biol 50: 69–78PubMedCrossRefGoogle Scholar
  50. Hirsh D, Oppenheim D, Klass M (1976) Development of the reproductive system of C. elegans. Dev Biol 49: 200–219PubMedCrossRefGoogle Scholar
  51. Hodgkin J, Horvitz HR, Brenner S (1979) Nondisjunction mutants of the nematode C. elegans. Genetics 91: 67–94PubMedGoogle Scholar
  52. Horvitz, HR (1988) Genetics of cell lineage. In: Wood WB (ed) The nematode Caenorhabditis elegans. Cold Spring Harbor Press, Cold Spring Harbor, New YorkGoogle Scholar
  53. Howell AM, Rose AM (1990) Essential genes in the hDf6 region of chromosome I of Caenorhabditis elegans. Genetics 126: 583–592PubMedGoogle Scholar
  54. Hyman AA (1989) Centrosome movement in the early divisions of Caenorhabditis elegans: a cortical site determining centrosome position. J Cell Biol 109: 1185–1193PubMedCrossRefGoogle Scholar
  55. Hyman AA, White JG (1987) Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans. J Cell Biol 105: 2123–2135PubMedCrossRefGoogle Scholar
  56. Illmensee K, Mahowald AP (1974) Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proc Natl Acad Sci USA 71: 1016–1020Google Scholar
  57. Isnenghi E, Cassada R, Smith K, Denich K, Radnia K, von Ehrenstein G (1983) Maternal effects and temperature-sensitive period of mutations affecting embryogenesis in Caenorhabditis elegans. Dev Biol 98: 465–480PubMedCrossRefGoogle Scholar
  58. Ito K, McGhee JD (1987) Parental DNA strands segregate randomly doringGoogle Scholar
  59. embryonic development of Caenorhabditis elegans. Cell 49:329–336Google Scholar
  60. Kemphues KJ (1989) Caenorhabditis. In: Glover DM, Hames BD (eds) Genes andGoogle Scholar
  61. embryos. IRL Press, OxfordGoogle Scholar
  62. Kemphues KJ, Kusch M, Wolf N (1988a) Maternal-effect lethal mutations on linkage group II of Caenorhabditis elegans. Genetics 120: 977–986PubMedGoogle Scholar
  63. Kemphues KJ, Priess JR, Morton DG, Cheng N (1988b) Identification of genes required for cytoplasmic localization in early Caenorhabditis elegans embryos. Cell 52: 311–320PubMedCrossRefGoogle Scholar
  64. Kemphues KJ, Wolf N, Wood WB, Hirsh D (1986) Two loci required for cytoplasmic organization in early embryos of Caenorhabditis elegans. Dev Biol 113: 449–460PubMedCrossRefGoogle Scholar
  65. Kenyon C (1986) A gene involved in the development of the posterior body region of C. elegans. Cell 46: 477–487PubMedCrossRefGoogle Scholar
  66. Kim SK, Horvitz HR (1990) The Caenorhabditis elegans gene lin-10 is broadly expressed while required specifically for the determination of vulval cell fates. Genes Dev 4: 357–371PubMedCrossRefGoogle Scholar
  67. Kimble J, Hirsh D (1979) Post-embryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev Biol 70: 396–417PubMedCrossRefGoogle Scholar
  68. Kimble J, Sharrock WJ (1983) Tissue-specific synthesis of yolk proteins in Caenorhabditis elegans. Dev Biol 96: 189–196PubMedCrossRefGoogle Scholar
  69. Kimble JE, White JG (1981) On the control of germ cell development in Caenorhabditis elegans. Dev Biol 81: 208–219PubMedCrossRefGoogle Scholar
  70. Kirby C, Kusch M, Kemphues K (1990) Mutations in par genes of Caenorhabditis elegans affect cytoplasmic reorganization during the first cell cycle. Dev Biol 142: 203–215PubMedCrossRefGoogle Scholar
  71. Kusch M, Edgar RS (1986) Genetic studies of unusual loci that affect body shape of the nematode Caenorhabditis elegans and may code for cuticle structural proteins. Genetics 113: 621–639PubMedGoogle Scholar
  72. Laufer JS, Bazzicalupo P, Wood WB (1980) Segregation of developmental potential in early embryos of Caenorhabditis elegans. Cell 19: 569–577PubMedCrossRefGoogle Scholar
  73. L’Hernault SW, Shakes DC, Ward S (1988) Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Genetics 120: 435–452PubMedGoogle Scholar
  74. Mains PE, Sulston IA, Wood WB (1990a) Dominant maternal-effect mutations causing embryonic lethality in Caenorhabditis elegans. Genetics 125: 351–369PubMedGoogle Scholar
  75. Mains PE, Kemphues KJ, Sprunger SA, Sulston IA, Wood WB (1990b) Mutations affecting the meiotic and mitotic divisions of the early Caenorhabditis elegans embryo. Genetics 126: 593–605PubMedGoogle Scholar
  76. McGhee JD (1992) Gut esterase expression in the nematode Caenorhabditis elegans. Adv Dev Biochem 1: 169–210Google Scholar
  77. Meneely PM, Herman RK (1979) Lethal, steriles and deficiencies in a region of the X chromosome of Caenorhabditis elegans. Genetics 92: 99–115PubMedGoogle Scholar
  78. Merrill P, Sweeton D, Wieschaus E (1988) Requirements for autosomal gene activity during precellular stages of Drosophila melanogaster. Development 104: 495–509PubMedGoogle Scholar
  79. Miwa J, Schierenberg E, Miwa S, von Ehrenstein G (1980) Genetics and mode of expression of temperature-sensitive mutations arresting embryonic development in Caenorhabditis elegans. Dev Biol 76: 160–174PubMedCrossRefGoogle Scholar
  80. Moerman DG, Benian GM, Waterston RH (1986) Molecular cloning of the muscle gene unc-22 in Caenorhabditis elegans by Tcl transposon tagging. Proc Natl Acad Sci USA 83: 2579–2583PubMedCrossRefGoogle Scholar
  81. Monk M (1990) Variation in epigenetic inheritance. Trends Genet 6: 110–114PubMedCrossRefGoogle Scholar
  82. Mori I, Moerman DG, Waterston RH (1988) Analysis of a mutator activityGoogle Scholar
  83. necessary for germline transposition and excision of Tel transposable elementsGoogle Scholar
  84. in Caenorhabditis elegans. Genetics 120:397–407Google Scholar
  85. Nigon V, Guerrier P, Monin H (1960) L’Architecture polaire de l’oeuf et les movements des constituants cellulaires au cour des premieres etapes du developpement chez quelques nematodes. Bull Biol Fr Belg 94: 132–201Google Scholar
  86. Nusslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature (London) 287: 795–801CrossRefGoogle Scholar
  87. Nusslein-Volhard C, Frohnhofer H, Lehmann R (1987) Determination of anterioposterior polarity in Drosophila. Science 238: 1675–1681PubMedCrossRefGoogle Scholar
  88. Park E-C, Horvitz HR (1986) Mutations with dominant effects on the behavior andGoogle Scholar
  89. morphology of the nematode Caenorhabditis elegans. Genetics 113:821–852 Perrimon N, Mohler D, Engstrom L, Mahowald AP (1986) X-linked female-sterileGoogle Scholar
  90. loci in Drosophila melanogaster. Genetics 113:695–712Google Scholar
  91. Perrimon N, Engstrom L, Mahowald AP (1989) Zygotic lethals with specific maternal effect phenotypes in Drosophila melanogaster. I. Loci on the X chromosome. Genetics 121: 333–352Google Scholar
  92. Pimpinelli S, Goday C (1989) Unusual kinetochores and chromatin diminution in Parascaris. Trends Genet 5: 310–315PubMedCrossRefGoogle Scholar
  93. Priess JR, Hirsh DI (1986) Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. Dev Biol 117: 156–173Google Scholar
  94. Priess JR, Thomson JN (1987) Cellular interactions in early Caenorhabditis elegans embryos. Cell 48: 241–250PubMedCrossRefGoogle Scholar
  95. Priess JR, Schnabel H, Schnable R (1987) The glp-1 locus and cellular interactions in early Caenorhabditis elegans embryos. Cell 51: 601–611PubMedCrossRefGoogle Scholar
  96. Roberts L (1990) The worm project. Science 248: 1310–1313PubMedCrossRefGoogle Scholar
  97. Rogalski TM, Riddle DL (1988) A Caenorhabditis elegans RNA polymerise II gene, ama-1 IV, and nearby essential genes. Genetics 118: 61–74PubMedGoogle Scholar
  98. Rogalski TM, Moerman DG, Baillie DL (1982) Essential genes and deficiencies in the unc-22 IV region of Caenorhabditis elegans. Genetics 102: 725–736PubMedGoogle Scholar
  99. Rosenbluth RE, Rogalski TM, Johnsen RC, Addison LM, Baillie DL (1988) Genomic organization in Caenorhabditis elegans: deficiency mapping on linkage group V (left). Genet Res 52: 105–118CrossRefGoogle Scholar
  100. Schauer IE, Wood WB (1990) Early C. elegans embryos are transcriptionally active. Development 110: 1303–1317PubMedGoogle Scholar
  101. Schierenberg E (1985) Cell determination during early embryogenesis of the nematode Caenorhabditis elegans. Cold Spring Harbor Symp Quant Biol 50: 59–68PubMedCrossRefGoogle Scholar
  102. Schierenberg E (1986) Developmental strategies during early embryogenesis of Caenorhabditis elegans. J Embryol Exp Morphol 97s: 31–44PubMedGoogle Scholar
  103. Schierenberg E (1987) Reversal of cellular polarity and early cell-cell interaction in the embryo of Caenorhabditis elegans. Dev Biol 122: 452–463PubMedCrossRefGoogle Scholar
  104. Schierenberg E (1988) Localization and segregation of lineage-specific cleavage potential in embryos of Caenorhabditis elegans. Wilhelm Roux’s Arch Dev Biol 197: 282–293CrossRefGoogle Scholar
  105. Schierenberg E (1989) Cytoplasmic determination and distribution of developmentalGoogle Scholar
  106. potential in the embryo of Caenorhabditis elegans. Bioessays 10:99–104 Schierenberg E, Wood WB (1985) Control of cell-cycle timing in early embryos ofGoogle Scholar
  107. Caenorhabditis elegans. Dev Biol 107:337–354Google Scholar
  108. Schierenberg E, Miwa J, von Ehrenstein G (1980) Cell lineages and developmental defects of temperature-sensitive embryonic arrest mutants in Caenorhabditis elegans. Dev Biol 76: 141–159PubMedCrossRefGoogle Scholar
  109. Schnabel R, Schnabel H (1990a) Early determination in the Caenorhabditis elegans embryo: a gene, cib-1, required to specify a set of stem-cell-like blastomeres. Development 108: 107–119PubMedGoogle Scholar
  110. Schnabel H, Schnabel R (1990b) An organ-specific differentiation gene, pha-1, from Caenorhabditis elegans. Science 250: 686–688PubMedCrossRefGoogle Scholar
  111. Seydoux G, Greenwald I (1989) Cell autonomy of lin-12 function in a cell fate decision in Caenorhabditis elegans. Cell 57: 1237–1245PubMedCrossRefGoogle Scholar
  112. Sigurdson DC, Spanier GJ, Herman RK (1984) Caenorhabditis elegans deficiency mapping. Genetics 108: 331–345Google Scholar
  113. Simpson VJ, Johnson TE, Hammen RF (1986) Caenorhabditis elegans DNA does not contain 5-methylcytosine at any time during development or aging. Nucl Acid Res 14: 6711–6717Google Scholar
  114. Sternberg PW, Horvitz HR (1984) The genetic control of cell lineage during nematode development. Annu Rev Genet 18: 489–524PubMedCrossRefGoogle Scholar
  115. Sternberg PW, Horvitz HR (1989) The combined action of two intercellular signalling pathways specifies three cell fates during vulval induction in Caenorhabditis elegans. Cell 58: 679–693PubMedCrossRefGoogle Scholar
  116. Stinchcomb DT, Shaw JE, Carr SH, Hirsh D (1985) Extrachromosomal DNA transformation of Caenorhabditis elegans. Mol Cell Biol 5: 3484–3496PubMedGoogle Scholar
  117. Storfer FA (1990) Contribution of embryonic gene expression to early embryogenesis in the nematode Caenorhabditis elegans: a genetic analysis. PhD Thesis, University of Colorado, Boulder, ColoradoGoogle Scholar
  118. Strome S (1986a) Fluorescence visualization of the distribution of microfilaments in gonads and early embryos of the nematode Caenorhabditis elegans. J Cell Biol 103: 2241–2252PubMedCrossRefGoogle Scholar
  119. Strome S (1986b) Asymmetric movements of cytoplasmic components inGoogle Scholar
  120. Caenorhabditis elegans zygotes. J Embryol Exp Morphol 97s:15–29Google Scholar
  121. Strome S (1989) Generation of cell diversity during early embryogenesis in theGoogle Scholar
  122. nematode Caenorhabditis elegans. Int Rev Cytol 114:81–124Google Scholar
  123. Strome S, Wood WB (1982) Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. Proc Natl Acad Sci USA 79: 1558–1562PubMedCrossRefGoogle Scholar
  124. Strome S, Wood WB (1983) Generation of asymmetry and segregation of germ-line granules in early Caenorhabditis elegans embryos. Cell 35: 15–25PubMedCrossRefGoogle Scholar
  125. Sulston JE (1988) Cell lineage. In: Wood WB (ed) The nematode Caenorhabditis Google Scholar
  126. elegans. Cold Spring Harbor Press, Cold Spring Harbor, New YorkGoogle Scholar
  127. Sulston JE, Brenner S (1974) The DNA of Caenorhabditis elegans. Genetics 77: 55Google Scholar
  128. Sulston JE, Horvitz HR (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56: 110–156PubMedCrossRefGoogle Scholar
  129. Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cellGoogle Scholar
  130. lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64–119Google Scholar
  131. Suzuki D (1970) Temperature-sensitive mutations in Drosophila melanogaster.Google Scholar
  132. Science 170:695–706Google Scholar
  133. Vanderslice R, Hirsh D (1976) Temperature-sensitive zygote defective mutants of Caenorhabditis elegans. Dev Biol 49: 236–249PubMedCrossRefGoogle Scholar
  134. Vavra SH, Carroll SB (1989) The zygotic control of Drosophila pair-rule gene expression I. A search for new pair-rule regulatory loci. Development 107: 663–672Google Scholar
  135. Ward S, Carrel JS (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73: 304–321PubMedCrossRefGoogle Scholar
  136. Waring DA, Kenyon C (1990) Selective silencing of cell communication influences anteroposterior pattern formation in Caenorhabditis elegans. Cell 60: 123–131PubMedCrossRefGoogle Scholar
  137. Wieschaus E, Sweeton, D (1988) Requirements for X-linked zygotic gene activity during cellularization of early Drosophila embryos. Development 104: 483493Google Scholar
  138. Wieschaus E, Nusslein-Volhard C, Jürgens G (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. Zygotic loci on the X-chromosome and fourth chromosome. Wilhelm Roux’s Arch Dev Biol 193: 296–307Google Scholar
  139. Wilkins AS (1986) Genetic analysis of animal development. John Wiley & Sons, New YorkGoogle Scholar
  140. Wolf N, Priess J, Hirsh D (1983) Segregation of germline granules in early embryos of Caenorhabditis elegans: an electron microscopic analysis. J Embryol Exp Morphol 73: 297–306PubMedGoogle Scholar
  141. Wood WB (ed) (1988a) The nematode Caenorhabditis elegans. Cold Spring Harbor Press, Cold Spring Harbor, New YorkGoogle Scholar
  142. Wood WB (1988b) Embryology. In: Wood WB (ed) The nematode Caenorhabditis elegans. Cold Spring Harbor Press, Cold Spring Harbor, New YorkGoogle Scholar
  143. Wood WB (1991) Reversal of handedness in C. elegans embryos: new evidence for extensive early cell interactions that determine cell fates. Nature (London) 349: 536–538CrossRefGoogle Scholar
  144. Wood WB, Hecht R, Carr S, Vanderslice R, Wolf N, Hirsh D (1980) Parental effects and phenotypic characterization of mutations that affect early development in Caenorhabditis elegans. Dev Biol 74: 446–469PubMedCrossRefGoogle Scholar
  145. Wood WB, Schierenberg E, Strome S (1984) Localization and determination in early embryos of Caenorhabditis elegans. UCLA Symp Mol Biol 19: 37–49Google Scholar
  146. Yamaguchi Y, Murakami K, Furusawa M, Miwa J (1983) Germline-specific antigens identified by monoclonal antibodies in the nematode Caenorhabditis elegans. Dev Growth Differ 25: 121–131CrossRefGoogle Scholar
  147. Yochem J, Greenwald I (1989) glp-1 and lin-12, genes implicated in distinct cell-cell interactions in Caenorhabditis elegans, encode similar transmembrane proteins. Cell 58: 553–563Google Scholar

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© Springer-Verlag Berlin Heidelberg 1992

Authors and Affiliations

  1. 1.Department of Medical BiochemistryUniversity of CalgaryCalgaryCanada

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