Advertisement

Wilhelm Roux's archives of developmental biology

, Volume 193, Issue 5, pp 296–307 | Cite as

Mutations affecting the pattern of the larval cuticle inDrosophila melanogaster

III. Zygotic loci on the X-chromosome and fourth chromosome
  • E. Wieschaus
  • C. Nüsslein-Volhard
  • Gerd Jürgens
Article

Summary

In order to identify X-chromosomal genes required inDrosophila for early patterning and morphogenesis, we examined embryos hemizygous for EMS-induced lethal mutations to determine which of those mutations cause gross morphological defects. Embryos from 2711 lethal lines, corresponding to 3255 lethal point mutations were studied. Only 21% caused death during embryogenesis and of these, only one-sixth, or 3% of the total lethals, were associated with defects visible in the final cuticle pattern. Of the 114 point mutants causing visible cuticle defects, 76 could be assigned to 14 complementation groups. An additional 25 mutations mapping to regions of the X-chromosome not covered by male fertile duplications were assigned to six complementation groups based on similarities of map position and phenotype. Thirteen mutations could not be assigned to complementation groups. All mutations allowed normal development through the cellular blastoderm stage, the first defects associated with the earliest acting loci being observed shortly after the onset of gastrulation. The phenotypes of the various loci range from alterations in segment pattern or early morphogenetic movements to defects in final pigmentation and denticle morphology.

Cuticle preparations were also examined for 63 deletions spanning in total 74% of the X-chromosome, as well as for 8 deletions and point mutations derived in saturation mutagenesis screens of the fourth chromosome (Hochman 1976). With the exception of defects in head morphology and defects in cuticle differentiation, none of the hemizygous deletions showed phenotypes other than those predicted by point mutations known to lie in those regions. No deletion caused new or unknown alterations in gastrulation, segmentation or cuticle pattern.These results suggest that the number of genes required zygotically for normal embryonic patterning is small and that most, if not all such loci, are represented by point mutations in our collection.

Key words

Drosophila Larval cuticle Pattern formation Embryonic lethal mutations 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson KV, Lengyel JA (1979) Rates of synthesis of major classes of RNA inDrosophila embryos. Dev Biol 70:217–231Google Scholar
  2. Bridges CB (1938) A revised map of the salivary gland X-chromosome. J Heredity 29:11Google Scholar
  3. Campos-Ortega JA, Jimenez F (1980) The effect of X-chromosome deficiencies in neurogenesis inDrosophila. In: Siddiqi O, Babu P, Hall LM, Hall JC (eds) Development and neurobiology ofDrosophila. Plenum Press, New York, pp 201–222Google Scholar
  4. Craymer L, Roy E (1980) New mutants-Drosophila melanogaster. Dros Inf Serv 55:200–204Google Scholar
  5. Ede DA (1956a) Studies on the lethal effects of some genetic lethal factors on the embryonic development ofDrosophila melanogaster. I. A preliminary survey of some sex-linked lethal stocks and an analysis of the mutant Lff 11. Arch Entwicklungsmech Organ 148:416–436Google Scholar
  6. Ede DA (1956b) Studies on the lethal effects of some genetic lethal factors on the embryonic development ofDrosophila melanogaster. II. An analysis of the mutant X-2. Arch Entwicklungsmech Organ 148:437–451Google Scholar
  7. Ede DA (1956b) Studies on the effects of some genetic lethal factors on the embryonic development ofDrosophila melanogaster. III. An analysis of the mutant X-27. Arch Entwicklungsmech Organ 149:88–100Google Scholar
  8. Ede DA (1956d) Studies on the effects of some genetic lethal factors on the embryonic development ofDrosophila melanogaster. IV. An analysis of the mutant X-20. Arch Entwicklungsmech Organ 149:101–144Google Scholar
  9. Garcia-Bellido A, Moscosco del Prado J (1979) Genetic analysis of maternal information inDrosophila. Nature 278:346–348Google Scholar
  10. Hadorn E (1955) Letalfaktoren in ihrer Bedeutung für Erbpathologie und Genphysiologie der Entwicklung. Thieme, StuttgartGoogle Scholar
  11. Hadorn E, Chen PS (1952) Untersuchungen zur Phasenspezifität der Wirkung von Letalfaktoren beiDrosophila melanogaster. Arch Julius Klaus-Stift. 27:147–163Google Scholar
  12. Hochman B (1976) The fourth chromosome ofDrosophila melanogaster. In: Ashburner M, Novitski E (eds) The genetics and biology ofDrosophila, vol 1b. Academic Press, New YorkGoogle Scholar
  13. Jan LY, Jan NJ (1982) Antibodies to horseradish peroxidase as specific neuronal markers inDrosophila and grasshopper embryos. PNAS (USA) 79:2700–2704Google Scholar
  14. Jimenez F, Campos-Ortega JA (1979) A region of theDrosophila genome necessary for CNS development. Nature 282:310–312Google Scholar
  15. Judd BH, Shen MW, Kaufman TC (1972) The anatomy and function of a segment of the X-chromosome ofDrosophila melanogaster. Genetics 71:139–156Google Scholar
  16. Jürgens C, Wieschaus E, Nüsslein-Volhard C, Kluding M (1984) Mutations affecting the pattern of the larval cuticle inDrosophila melanogaster. II. Zygotic loci on the third chromosome. Wilhelm Roux's Arch 193:283–295Google Scholar
  17. Lamb MM, Laird CD (1976) Increase in nuclear poly(A)-containing RNA at syncytial blastoderm inDrosophila melanogaster embryos. Dev Biol 52:31–42Google Scholar
  18. Lefevre G (1974) The relationship between genes and polytene chromosome bands. Ann Rev Genet 8:51–62Google Scholar
  19. Lewis EB, Bacher F (1968) A method of feeding ethyl methane sulfonate (EMS) toDrosophila males. Dros Inf Serv 43:193Google Scholar
  20. Lindsley DL, Grell EH (1968) Genetic variations ofDrosophila melanogaster. Carnegie Inst Wash Publ 627Google Scholar
  21. McKnight SL, Miller OL Jr (1976) Ultrastructural patterns of RNA synthesis during early embryogenesis ofDrosophila melanogaster Cell 8:305–319Google Scholar
  22. Merriam JR, Duffy C (1972) First multiple seven now contains snx2 for better balancing. Dros Inf Serv 48:43Google Scholar
  23. Muller HJ (1928) The measurement of gene mutation rate inDrosophila, its high variability and its dependence upon temperature. Genetics 13:279–357Google Scholar
  24. Nicklas JA, Cline TW (1983) Vital genes that flank Sex-lethal, an X-linked sex-determinating gene ofDrosophila melanogaster. Genetics 103:617–631Google Scholar
  25. Nüsslein-Volhard C (1977) A rapid method for screening eggs from singleDrosophila females. Dros Inf Serv 52:166Google Scholar
  26. Nüsslein-Volhard, C, Wieschaus E (1980) Mutations affecting segment number and polarity inDrosophila. Nature 287:795–801Google Scholar
  27. Nüsslein-Volhard C, Wieschaus E, Kluding M (1984) Mutations affecting the pattern of the larval cuticle inDrosophila melanogaster. I. Zygotic loci on the second chromosome. Wilhelm Roux's Arch 193:267–282Google Scholar
  28. Poulson DF (1940) The effects of certain X-chromosome deficiencies on the embryonic development ofDrosophila melanogaster. J Exp Zool 83:235–271Google Scholar
  29. Schalet A, Lefevre G (1976) The proximal region of the X-chromosome in biology and genetics ofDrosophila, Ashburner M, Novitski E (eds) vol 1b. Academic Press, New York, pp 848–902Google Scholar
  30. Scriba MEL (1964) Beeinflussung der frühen Embryonalentwicklung vonDrosophila melanogaster durch Chromosomenaberrationen. Zool Jahrb Abt Anat Ontog Tiere 81:435–490Google Scholar
  31. Scriba MEL (1967) Embryonale Entwicklungsstörungen bein Defizienz und Tetraploidie des 2. Chromosoms vonDrosophila melanogaster. Arch Entwicklungsmech Organ 159:314–315Google Scholar
  32. Scriba MEL (1969) Embryonale Entwicklungsstörungen bei Nullosomie und Tetrasomie des 3. Chromosoms vonDrosophila melanogaster. Dev Biol 19:160–171Google Scholar
  33. Sina BJ, Pellegrini M (1982) Genomic clones coding for some of the initial genes expressed duringDrosophila development. Proc Natl Acad Sci USA 79:7351–7355Google Scholar
  34. Spencer WP, Stern C (1948) Experiments to test the validity of the linear r-dose/mutation frequency relation inDrosophila at low dosage. Genetics 33:43–74Google Scholar
  35. Van der Meer J (1977) Optical clean and permanent whole mount preparations for phase-contrase microscopy of cuticle structures of insect larvae. Dros Inf Serv 52:160Google Scholar
  36. White K (1980) Defective neural development inDrosophila melanogaster embryos deficient for the tip of the X-chromosome. Dev Biol 80:332–344Google Scholar
  37. Wright TRF (1960) The phenogenetics of the embryonic mutant lethalmyospheroid inDrosophila melanogaster. J Exp Zool 143:77–99Google Scholar
  38. Wright TRF (1970) The genetics of embryogenesis inDrosophila. Adv Genet 15:262–385Google Scholar
  39. Zalokar M (1976) Autoradiographic study of protein and RNA formation during early development ofDrosophila eggs. Dev Biol 49:425–437Google Scholar
  40. Zalokar M, Erk I (1977) Phase-partition fixation and staining ofDrosophila eggs. Stain Technol 52:89–95Google Scholar

Copyright information

© Springer-Verlag 1984

Authors and Affiliations

  • E. Wieschaus
    • 1
    • 2
  • C. Nüsslein-Volhard
    • 1
    • 2
  • Gerd Jürgens
    • 1
    • 2
  1. 1.European Molecular Biology LaboratoryHeidelbergFederal Republic of Germany
  2. 2.Department of BiologyPrinceton UniversityPrincetonUSA

Personalised recommendations