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. 1993 Dec;135(4):1047–1062. doi: 10.1093/genetics/135.4.1047

Segmental Polarity in Drosophila Melanogaster: Genetic Dissection of Fused in a Suppressor of Fused Background Reveals Interaction with Costal-2

T Preat 1, P Therond 1, B Limbourg-Bouchon 1, A Pham 1, H Tricoire 1, D Busson 1, C Lamour-Isnard 1
PMCID: PMC1205737  PMID: 8307322

Abstract

fused (fu) is a segment polarity gene that encodes a putative serine/threonine kinase. A complete suppressor of the embryonic and adult phenotypes of fu mutants, Suppressor of fused (Su(fu)), was previously described. The amorphic Su(fu) mutation is viable and displays no phenotype by itself. We have used this suppressor as a tool to perform a genetic dissection of the fu gene. Analysis of the interaction between Su(fu) and 33 fu alleles shows that they belong to three different classes. Defects due to class I fu alleles are fully suppressed by Su(fu). Class II fu alleles lead to a new segment polarity phenotype in interaction with Su(fu). This phenotype corresponds to embryonic and adult anomalies similar to those displayed by the segment polarity mutant costal-2 (cos-2). Class II alleles are recessive to class I alleles in a fu[I]/fu[II];Su(fu)/Su(fu) combination. Class 0 alleles, like class I alleles, confer a normal segmentation phenotype in interaction with Su(fu). However class II alleles are dominant over class 0 alleles in a fu[0]/fu[II];Su(fu)/Su(fu) combination. Alleles of class I and II correspond to small molecular events, which may leave part of the Fu protein intact. On the contrary, class 0 alleles correspond to large deletions. Several class I and class II fu mutations have been mapped, and three mutant alleles were sequenced. These data suggest that class I mutations affect the catalytic domain of the putative Fu kinase and leave the carboxy terminal domain intact, whereas predicted class II proteins have an abnormal carboxy terminal domain. Su(fu) enhances the cos-2 phenotype and cos-2 mutations interact with fu in a way similar to Su(fu). All together these results suggest that a close relationship might exist between fu, Su(fu) and cos-2 throughout development. We thus propose a model where the Fu(+) kinase is a posterior inhibitor of Costal-2(+) while Su(fu)(+) is an activator of Costal-2(+). The expression pattern of wingless and engrailed in fu and fu;Su(fu) embryos is in accordance with this interpretation.

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Selected References

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  1. Busson D., Gans M., Komitopoulou K., Masson M. Genetic Analysis of Three Dominant Female-Sterile Mutations Located on the X Chromosome of DROSOPHILA MELANOGASTER. Genetics. 1983 Oct;105(2):309–325. doi: 10.1093/genetics/105.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Gans M., Audit C., Masson M. Isolation and characterization of sex-linked female-sterile mutants in Drosophila melanogaster. Genetics. 1975 Dec;81(4):683–704. doi: 10.1093/genetics/81.4.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Garcia-Bellido A., Ripoll P., Morata G. Developmental compartmentalisation of the wing disk of Drosophila. Nat New Biol. 1973 Oct 24;245(147):251–253. doi: 10.1038/newbio245251a0. [DOI] [PubMed] [Google Scholar]
  4. Gausz J., Bencze G., Gyurkovics H., Ashburner M., Ish-Horowicz D., Holden J. J. Genetic Characterization of the 87c Region of the Third Chromosome of DROSOPHILA MELANOGASTER. Genetics. 1979 Dec;93(4):917–934. doi: 10.1093/genetics/93.4.917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Hanks S. K., Quinn A. M., Hunter T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science. 1988 Jul 1;241(4861):42–52. doi: 10.1126/science.3291115. [DOI] [PubMed] [Google Scholar]
  6. Hidalgo A., Ingham P. Cell patterning in the Drosophila segment: spatial regulation of the segment polarity gene patched. Development. 1990 Sep;110(1):291–301. doi: 10.1242/dev.110.1.291. [DOI] [PubMed] [Google Scholar]
  7. Hooper J. E., Scott M. P. The molecular genetic basis of positional information in insect segments. Results Probl Cell Differ. 1992;18:1–48. doi: 10.1007/978-3-540-47191-2_1. [DOI] [PubMed] [Google Scholar]
  8. Ingham P. W. Segment polarity genes and cell patterning within the Drosophila body segment. Curr Opin Genet Dev. 1991 Aug;1(2):261–267. doi: 10.1016/s0959-437x(05)80080-2. [DOI] [PubMed] [Google Scholar]
  9. Limbourg-Bouchon B., Busson D., Lamour-Isnard C. Interactions between fused, a segment-polarity gene in Drosophila, and other segmentation genes. Development. 1991 Jun;112(2):417–429. doi: 10.1242/dev.112.2.417. [DOI] [PubMed] [Google Scholar]
  10. Mariol M. C., Preat T., Limbourg-Bouchon B. Molecular cloning of fused, a gene required for normal segmentation in the Drosophila melanogaster embryo. Mol Cell Biol. 1987 Sep;7(9):3244–3251. doi: 10.1128/mcb.7.9.3244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Martinez Arias A. A cellular basis for pattern formation in the insect epidermis. Trends Genet. 1989 Aug;5(8):262–267. doi: 10.1016/0168-9525(89)90099-1. [DOI] [PubMed] [Google Scholar]
  12. Martinez-Arias A. The development of fused- embryos of Drosophila melanogaster. J Embryol Exp Morphol. 1985 Jun;87:99–114. [PubMed] [Google Scholar]
  13. Martizez Arias A., Baker N. E., Ingham P. W. Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo. Development. 1988 May;103(1):157–170. doi: 10.1242/dev.103.1.157. [DOI] [PubMed] [Google Scholar]
  14. Nüsslein-Volhard C., Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature. 1980 Oct 30;287(5785):795–801. doi: 10.1038/287795a0. [DOI] [PubMed] [Google Scholar]
  15. Perrimon N., Gans M. Clonal analysis of the tissue specificity of recessive female-sterile mutations of Drosophila melanogaster using a dominant female-sterile mutation Fs(1)K1237. Dev Biol. 1983 Dec;100(2):365–373. doi: 10.1016/0012-1606(83)90231-2. [DOI] [PubMed] [Google Scholar]
  16. Perrimon N., Mahowald A. P. Multiple functions of segment polarity genes in Drosophila. Dev Biol. 1987 Feb;119(2):587–600. doi: 10.1016/0012-1606(87)90061-3. [DOI] [PubMed] [Google Scholar]
  17. Préat T., Thérond P., Lamour-Isnard C., Limbourg-Bouchon B., Tricoire H., Erk I., Mariol M. C., Busson D. A putative serine/threonine protein kinase encoded by the segment-polarity fused gene of Drosophila. Nature. 1990 Sep 6;347(6288):87–89. doi: 10.1038/347087a0. [DOI] [PubMed] [Google Scholar]
  18. Siegfried E., Ambrosio L., Perrimon N. Serine/threonine protein kinases in Drosophila. Trends Genet. 1990 Nov;6(11):357–362. doi: 10.1016/0168-9525(90)90277-d. [DOI] [PubMed] [Google Scholar]
  19. Simpson P., Grau Y. The segment polarity gene costal-2 in Drosophila. II. The origin of imaginal pattern duplications. Dev Biol. 1987 Jul;122(1):201–209. doi: 10.1016/0012-1606(87)90345-9. [DOI] [PubMed] [Google Scholar]
  20. Thérond P., Mastrippolito R., Tricoire H. A new deficiency mapping technique using the SOFI detector. Biotechniques. 1992 Feb;12(2):252–257. [PubMed] [Google Scholar]
  21. Whittle J. R. Clonal analysis of a genetically caused duplication of the anterior wing in Drosophila melanogaster. Dev Biol. 1976 Jul 15;51(2):257–268. doi: 10.1016/0012-1606(76)90142-1. [DOI] [PubMed] [Google Scholar]
  22. Wilkins A. S., Gubb D. Pattern formation in the embryo and imaginal discs of Drosophila: what are the links? Dev Biol. 1991 May;145(1):1–12. doi: 10.1016/0012-1606(91)90208-k. [DOI] [PubMed] [Google Scholar]

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