Abstract
We have analyzed pregastrulation cleavage patterns in Caenorhabditis elegans embryos homozygous for various chromosomal deficiencies. By two different estimates these deficiencies represent between 37 and 49% of the genome, including the entire X chromosome and substantial portions of each of the five autosomes. Among these genomic regions, we find none whose absence causes defects in pregastrulation cleavage patterns. We can conclude that there are at most very few genes whose transcription after fertilization is required for normal early patterning of cell divisions. We also scored terminal phenotypes of the homozygous deficiency embryos for stage of arrest and for expression of three tissue-specific differentiation markers. Based on these phenotypes, we have identified regions of the genome that are required for completion of cell proliferation, expression of gut differentiation and entry into morphogenesis. Somewhat surprisingly, embryos in which cell proliferation is arrested at less than 20% of the normal cell number can nevertheless initiate morphogenesis and undergo elongation to the twofold stage. Our results are consistent with the view that many early events in C. elegans embryogenesis are controlled exclusively by maternally produced gene products. However, they are also consistent with the likely possibility that, at least in some deficiency embryos, although cleavage patterns may be normal, blastomere identities are not. In this respect the early cleavages may differ from later lineages, in which cell division patterns appear to be characteristic of cell identity.
Full Text
The Full Text of this article is available as a PDF (3.5 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Albertson D. G., Thomson J. N. The kinetochores of Caenorhabditis elegans. Chromosoma. 1982;86(3):409–428. doi: 10.1007/BF00292267. [DOI] [PubMed] [Google Scholar]
- Bowerman B., Eaton B. A., Priess J. R. skn-1, a maternally expressed gene required to specify the fate of ventral blastomeres in the early C. elegans embryo. Cell. 1992 Mar 20;68(6):1061–1075. doi: 10.1016/0092-8674(92)90078-q. [DOI] [PubMed] [Google Scholar]
- Bucher E. A., Greenwald I. A genetic mosaic screen of essential zygotic genes in Caenorhabditis elegans. Genetics. 1991 Jun;128(2):281–292. doi: 10.1093/genetics/128.2.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Clark D. V., Rogalski T. M., Donati L. M., Baillie D. L. The unc-22(IV) region of Caenorhabditis elegans: genetic analysis of lethal mutations. Genetics. 1988 Jun;119(2):345–353. doi: 10.1093/genetics/119.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coulson A., Sulston J., Brenner S., Karn J. Toward a physical map of the genome of the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7821–7825. doi: 10.1073/pnas.83.20.7821. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coulson A., Waterston R., Kiff J., Sulston J., Kohara Y. Genome linking with yeast artificial chromosomes. Nature. 1988 Sep 8;335(6186):184–186. doi: 10.1038/335184a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Edgar L. G., Wolf N., Wood W. B. Early transcription in Caenorhabditis elegans embryos. Development. 1994 Feb;120(2):443–451. doi: 10.1242/dev.120.2.443. [DOI] [PubMed] [Google Scholar]
- Greenwald I., Coulson A., Sulston J., Priess J. Correlation of the physical and genetic maps in the lin-12 region of Caenorhabditis elegans. Nucleic Acids Res. 1987 Mar 11;15(5):2295–2307. doi: 10.1093/nar/15.5.2295. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hecht R. M., Gossett L. A., Jeffery W. R. Ontogeny of maternal and newly transcribed mRNA analyzed by in situ hybridization during development of Caenorhabditis elegans. Dev Biol. 1981 Apr 30;83(2):374–379. doi: 10.1016/0012-1606(81)90484-x. [DOI] [PubMed] [Google Scholar]
- Herman R. K., Albertson D. G., Brenner S. Chromosome rearrangements in Caenorhabditis elegans. Genetics. 1976 May;83(1):91–105. doi: 10.1093/genetics/83.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herman R. K. Crossover suppressors and balanced recessive lethals in Caenorhabditis elegans. Genetics. 1978 Jan;88(1):49–65. doi: 10.1093/genetics/88.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- Mains P. E., Sulston I. A., Wood W. B. Dominant maternal-effect mutations causing embryonic lethality in Caenorhabditis elegans. Genetics. 1990 Jun;125(2):351–369. doi: 10.1093/genetics/125.2.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mello C. C., Draper B. W., Krause M., Weintraub H., Priess J. R. The pie-1 and mex-1 genes and maternal control of blastomere identity in early C. elegans embryos. Cell. 1992 Jul 10;70(1):163–176. doi: 10.1016/0092-8674(92)90542-k. [DOI] [PubMed] [Google Scholar]
- Meneely P. M., Herman R. K. Lethals, steriles and deficiencies in a region of the X chromosome of Caenorhabditis elegans. Genetics. 1979 May;92(1):99–115. doi: 10.1093/genetics/92.1.99. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meneely P. M., Herman R. K. Suppression and function of X-linked lethal and sterile mutations in Caenorhabditis elegans. Genetics. 1981 Jan;97(1):65–84. doi: 10.1093/genetics/97.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Merrill P. T., Sweeton D., Wieschaus E. Requirements for autosomal gene activity during precellular stages of Drosophila melanogaster. Development. 1988 Nov;104(3):495–509. doi: 10.1242/dev.104.3.495. [DOI] [PubMed] [Google Scholar]
- Miwa J., Schierenberg E., Miwa S., von Ehrenstein G. Genetics and mode of expression of temperature-sensitive mutations arresting embryonic development in Caenorhabditis elegans. Dev Biol. 1980 Apr;76(1):160–174. doi: 10.1016/0012-1606(80)90369-3. [DOI] [PubMed] [Google Scholar]
- Rogalski T. M., Moerman D. G., Baillie D. L. Essential genes and deficiencies in the unc-22 IV region of Caenorhabditis elegans. Genetics. 1982 Dec;102(4):725–736. doi: 10.1093/genetics/102.4.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schauer I. E., Wood W. B. Early C. elegans embryos are transcriptionally active. Development. 1990 Dec;110(4):1303–1317. doi: 10.1242/dev.110.4.1303. [DOI] [PubMed] [Google Scholar]
- Schierenberg E., Miwa J., von Ehrenstein G. Cell lineages and developmental defects of temperature-sensitive embryonic arrest mutants in Caenorhabditis elegans. Dev Biol. 1980 Apr;76(1):141–159. doi: 10.1016/0012-1606(80)90368-1. [DOI] [PubMed] [Google Scholar]
- Schnabel R., Schnabel H. Early determination in the C. elegans embryo: a gene, cib-1, required to specify a set of stem-cell-like blastomeres. Development. 1990 Jan;108(1):107–119. doi: 10.1242/dev.108.Supplement.107. [DOI] [PubMed] [Google Scholar]
- Sigurdson D. C., Spanier G. J., Herman R. K. Caenorhabditis elegans deficiency mapping. Genetics. 1984 Oct;108(2):331–345. doi: 10.1093/genetics/108.2.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
- St Johnston D., Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell. 1992 Jan 24;68(2):201–219. doi: 10.1016/0092-8674(92)90466-p. [DOI] [PubMed] [Google Scholar]
- 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]
- Sulston J., Du Z., Thomas K., Wilson R., Hillier L., Staden R., Halloran N., Green P., Thierry-Mieg J., Qiu L. The C. elegans genome sequencing project: a beginning. Nature. 1992 Mar 5;356(6364):37–41. doi: 10.1038/356037a0. [DOI] [PubMed] [Google Scholar]
- Trent C., Wood W. B., Horvitz H. R. A novel dominant transformer allele of the sex-determining gene her-1 of Caenorhabditis elegans. Genetics. 1988 Sep;120(1):145–157. doi: 10.1093/genetics/120.1.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vanderslice R., Hirsh D. Temperature-sensitive zygote defective mutants of Caenorhabditis elegans. Dev Biol. 1976 Mar;49(1):236–249. doi: 10.1016/0012-1606(76)90269-4. [DOI] [PubMed] [Google Scholar]
- Vavra S. H., Carroll S. B. The zygotic control of Drosophila pair-rule gene expression. I. A search for new pair-rule regulatory loci. Development. 1989 Nov;107(3):663–672. doi: 10.1242/dev.107.3.663. [DOI] [PubMed] [Google Scholar]
- Wieschaus E., Sweeton D. Requirements for X-linked zygotic gene activity during cellularization of early Drosophila embryos. Development. 1988 Nov;104(3):483–493. doi: 10.1242/dev.104.3.483. [DOI] [PubMed] [Google Scholar]
- 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]
