Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1995 Feb;139(2):549–559. doi: 10.1093/genetics/139.2.549

Control of Cleavage Spindle Orientation in Caenorhabditis Elegans: The Role of the Genes Par-2 and Par-3

N N Cheng 1, C M Kirby 1, K J Kemphues 1
PMCID: PMC1206366  PMID: 7713417

Abstract

Polarized asymmetric divisions play important roles in the development of plants and animals. The first two embryonic cleavages of Caenorhabditis elegans provide an opportunity to study the mechanisms controlling polarized asymmetric divisions. The first cleavage is unequal, producing daughters with different sizes and fates. The daughter blastomeres divide with different orientations at the second cleavage; the anterior blastomere divides equally across the long axis of the egg, whereas the posterior blastomere divides unequally along the long axis. We report here the results of our analysis of the genes par-2 and par-3 with respect to their contribution to the polarity of these division. Strong loss-of-function mutations in both genes lead to an equal first cleavage and an altered second cleavage. Interestingly, the mutations exhibit striking gene-specific differences at the second cleavage. The par-2 mutations lead to transverse spindle orientations in both blastomeres, whereas par-3 mutations lead to longitudinal spindle orientations in both blastomeres. The spindle orientation defects correlate with defects in centrosome movements during both the first and the second cell cycle. Temperature shift experiments with par-2(it5ts) indicate that the par-2(+) activity is not required after the two-cell stage. Analysis of double mutants shows that par-3 is epistatic to par-2. We propose a model wherein par-2(+) and par-3(+) act in concert during the first cell cycle to affect asymmetric modification of the cytoskeleton. This polar modification leads to different behaviors of centrosomes in the anterior and posterior and leads ultimately to blastomere-specific spindle orientations at the second cleavage.

Full Text

The Full Text of this article is available as a PDF (3.2 MB).

Selected References

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

  1. Drubin D. G. Development of cell polarity in budding yeast. Cell. 1991 Jun 28;65(7):1093–1096. doi: 10.1016/0092-8674(91)90001-f. [DOI] [PubMed] [Google Scholar]
  2. Golden J. W., Riddle D. L. A pheromone-induced developmental switch in Caenorhabditis elegans: Temperature-sensitive mutants reveal a wild-type temperature-dependent process. Proc Natl Acad Sci U S A. 1984 Feb;81(3):819–823. doi: 10.1073/pnas.81.3.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Hill D. P., Strome S. 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. 1990 Jan;108(1):159–172. doi: 10.1242/dev.108.1.159. [DOI] [PubMed] [Google Scholar]
  4. Hirsh D., Oppenheim D., Klass M. Development of the reproductive system of Caenorhabditis elegans. Dev Biol. 1976 Mar;49(1):200–219. doi: 10.1016/0012-1606(76)90267-0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Hyman A. A. Centrosome movement in the early divisions of Caenorhabditis elegans: a cortical site determining centrosome position. J Cell Biol. 1989 Sep;109(3):1185–1193. doi: 10.1083/jcb.109.3.1185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hyman A. A., White J. G. Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans. J Cell Biol. 1987 Nov;105(5):2123–2135. doi: 10.1083/jcb.105.5.2123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. 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]
  11. Levitan D. J., Boyd L., Mello C. C., Kemphues K. J., Stinchcomb D. T. par-2, a gene required for blastomere asymmetry in Caenorhabditis elegans, encodes zinc-finger and ATP-binding motifs. Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):6108–6112. doi: 10.1073/pnas.91.13.6108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Mains P. E., Kemphues K. J., Sprunger S. A., Sulston I. A., Wood W. B. Mutations affecting the meiotic and mitotic divisions of the early Caenorhabditis elegans embryo. Genetics. 1990 Nov;126(3):593–605. doi: 10.1093/genetics/126.3.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Palmer R. E., Sullivan D. S., Huffaker T., Koshland D. Role of astral microtubules and actin in spindle orientation and migration in the budding yeast, Saccharomyces cerevisiae. J Cell Biol. 1992 Nov;119(3):583–593. doi: 10.1083/jcb.119.3.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Schierenberg E. Cell determination during early embryogenesis of the nematode Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol. 1985;50:59–68. doi: 10.1101/sqb.1985.050.01.010. [DOI] [PubMed] [Google Scholar]
  15. Schroeder T. E. Fourth cleavage of sea urchin blastomeres: microtubule patterns and myosin localization in equal and unequal cell divisions. Dev Biol. 1987 Nov;124(1):9–22. doi: 10.1016/0012-1606(87)90454-4. [DOI] [PubMed] [Google Scholar]
  16. Strome S. Determination of cleavage planes. Cell. 1993 Jan 15;72(1):3–6. doi: 10.1016/0092-8674(93)90041-n. [DOI] [PubMed] [Google Scholar]
  17. Strome S., Wood W. B. Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell. 1983 Nov;35(1):15–25. doi: 10.1016/0092-8674(83)90203-9. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Sulston J. E., Schierenberg E., White J. G., Thomson J. N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol. 1983 Nov;100(1):64–119. doi: 10.1016/0012-1606(83)90201-4. [DOI] [PubMed] [Google Scholar]
  20. Suzuki D. T. Temperature-sensitive mutations in Drosophila melanogaster. Science. 1970 Nov 13;170(3959):695–706. doi: 10.1126/science.170.3959.695. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. 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