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. 1996 Jan 15;15(2):334–343.

Functional hierarchy and phenotypic suppression among Drosophila homeotic genes: the labial and empty spiracles genes.

A Macías 1, G Morata 1
PMCID: PMC449948  PMID: 8617208

Abstract

The Drosophila homeotic cluster (HOM-C) is made up of eight genes, which specify the identity of cephalic, thoracic and abdominal segments. These genes can be ordered in a hierarchy which correlates with their position along the 5'-3' transcriptional direction. When they are absent, thoracic and abdominal body segments develop the same'ground' pattern, which is thoracic-like but also includes cephalic structures (sclerotic plates). We find that these plates are specified by the homeobox gene empty spiracles (ems) which is not a member of the HOM-C and which is expressed in all body segments. ems mutations, however, only produce defects in anterior head structures and the posterior spiracles. The ems product has the potential to induce sclerotic plates but this potential is suppressed by any of the HOM-C genes, including the labial gene, which we show to be the lowest ranking of the HOM-C hierarchy. This suppression does not occur at the transcriptional or translational level because the ems function is suppressed in cells containing the ems product. Thus, this appears to be the first case of phenotypic suppression operating in normal development. We propose that ems was originally a member of the HOM-C which escaped from the complex and has also acquired new functions during evolution.

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Selected References

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

  1. Akam M., Averof M., Castelli-Gair J., Dawes R., Falciani F., Ferrier D. The evolving role of Hox genes in arthropods. Dev Suppl. 1994:209–215. [PubMed] [Google Scholar]
  2. Akam M. Hox and HOM: homologous gene clusters in insects and vertebrates. Cell. 1989 May 5;57(3):347–349. doi: 10.1016/0092-8674(89)90909-4. [DOI] [PubMed] [Google Scholar]
  3. Bachiller D., Macías A., Duboule D., Morata G. Conservation of a functional hierarchy between mammalian and insect Hox/HOM genes. EMBO J. 1994 Apr 15;13(8):1930–1941. doi: 10.1002/j.1460-2075.1994.tb06462.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Busturia A., Morata G. Ectopic expression of homeotic genes caused by the elimination of the Polycomb gene in Drosophila imaginal epidermis. Development. 1988 Dec;104(4):713–720. doi: 10.1242/dev.104.4.713. [DOI] [PubMed] [Google Scholar]
  5. Capovilla M., Brandt M., Botas J. Direct regulation of decapentaplegic by Ultrabithorax and its role in Drosophila midgut morphogenesis. Cell. 1994 Feb 11;76(3):461–475. doi: 10.1016/0092-8674(94)90111-2. [DOI] [PubMed] [Google Scholar]
  6. Casanova J., Sánchez-Herrero E., Busturia A., Morata G. Double and triple mutant combinations of bithorax complex of Drosophila. EMBO J. 1987 Oct;6(10):3103–3109. doi: 10.1002/j.1460-2075.1987.tb02619.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Casanova J., Sánchez-Herrero E., Morata G. Identification and characterization of a parasegment specific regulatory element of the abdominal-B gene of Drosophila. Cell. 1986 Nov 21;47(4):627–636. doi: 10.1016/0092-8674(86)90627-6. [DOI] [PubMed] [Google Scholar]
  8. Chadwick R., McGinnis W. Temporal and spatial distribution of transcripts from the Deformed gene of Drosophila. EMBO J. 1987 Mar;6(3):779–789. doi: 10.1002/j.1460-2075.1987.tb04820.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chouinard S., Kaufman T. C. Control of expression of the homeotic labial (lab) locus of Drosophila melanogaster: evidence for both positive and negative autogenous regulation. Development. 1991 Dec;113(4):1267–1280. doi: 10.1242/dev.113.4.1267. [DOI] [PubMed] [Google Scholar]
  10. Cohen S. M., Jürgens G. Mediation of Drosophila head development by gap-like segmentation genes. Nature. 1990 Aug 2;346(6283):482–485. doi: 10.1038/346482a0. [DOI] [PubMed] [Google Scholar]
  11. Dalton D., Chadwick R., McGinnis W. Expression and embryonic function of empty spiracles: a Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev. 1989 Dec;3(12A):1940–1956. doi: 10.1101/gad.3.12a.1940. [DOI] [PubMed] [Google Scholar]
  12. Diederich R. J., Merrill V. K., Pultz M. A., Kaufman T. C. Isolation, structure, and expression of labial, a homeotic gene of the Antennapedia Complex involved in Drosophila head development. Genes Dev. 1989 Mar;3(3):399–414. doi: 10.1101/gad.3.3.399. [DOI] [PubMed] [Google Scholar]
  13. Duboule D., Dollé P. The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J. 1989 May;8(5):1497–1505. doi: 10.1002/j.1460-2075.1989.tb03534.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Duboule D., Morata G. Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet. 1994 Oct;10(10):358–364. doi: 10.1016/0168-9525(94)90132-5. [DOI] [PubMed] [Google Scholar]
  15. Duboule D. Patterning in the vertebrate limb. Curr Opin Genet Dev. 1991 Aug;1(2):211–216. doi: 10.1016/s0959-437x(05)80072-3. [DOI] [PubMed] [Google Scholar]
  16. Finkelstein R., Smouse D., Capaci T. M., Spradling A. C., Perrimon N. The orthodenticle gene encodes a novel homeo domain protein involved in the development of the Drosophila nervous system and ocellar visual structures. Genes Dev. 1990 Sep;4(9):1516–1527. doi: 10.1101/gad.4.9.1516. [DOI] [PubMed] [Google Scholar]
  17. Garcia-Fernández J., Holland P. W. Archetypal organization of the amphioxus Hox gene cluster. Nature. 1994 Aug 18;370(6490):563–566. doi: 10.1038/370563a0. [DOI] [PubMed] [Google Scholar]
  18. Gavis E. R., Lehmann R. Localization of nanos RNA controls embryonic polarity. Cell. 1992 Oct 16;71(2):301–313. doi: 10.1016/0092-8674(92)90358-j. [DOI] [PubMed] [Google Scholar]
  19. Gehring W. J., Affolter M., Bürglin T. Homeodomain proteins. Annu Rev Biochem. 1994;63:487–526. doi: 10.1146/annurev.bi.63.070194.002415. [DOI] [PubMed] [Google Scholar]
  20. González-Reyes A., Macías A., Morata G. Autocatalysis and phenotypic expression of Drosophila homeotic gene Deformed: its dependence on polarity and homeotic gene function. Development. 1992 Dec;116(4):1059–1068. doi: 10.1242/dev.116.4.1059. [DOI] [PubMed] [Google Scholar]
  21. González-Reyes A., Morata G. The developmental effect of overexpressing a Ubx product in Drosophila embryos is dependent on its interactions with other homeotic products. Cell. 1990 May 4;61(3):515–522. doi: 10.1016/0092-8674(90)90533-k. [DOI] [PubMed] [Google Scholar]
  22. González-Reyes A., Urquia N., Gehring W. J., Struhl G., Morata G. Are cross-regulatory interactions between homoeotic genes functionally significant? Nature. 1990 Mar 1;344(6261):78–80. doi: 10.1038/344078a0. [DOI] [PubMed] [Google Scholar]
  23. Graham A., Papalopulu N., Krumlauf R. The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell. 1989 May 5;57(3):367–378. doi: 10.1016/0092-8674(89)90912-4. [DOI] [PubMed] [Google Scholar]
  24. Guan K. L., Dixon J. E. Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal Biochem. 1991 Feb 1;192(2):262–267. doi: 10.1016/0003-2697(91)90534-z. [DOI] [PubMed] [Google Scholar]
  25. Hülskamp M., Pfeifle C., Tautz D. A morphogenetic gradient of hunchback protein organizes the expression of the gap genes Krüppel and knirps in the early Drosophila embryo. Nature. 1990 Aug 9;346(6284):577–580. doi: 10.1038/346577a0. [DOI] [PubMed] [Google Scholar]
  26. Jones B., McGinnis W. The regulation of empty spiracles by Abdominal-B mediates an abdominal segment identity function. Genes Dev. 1993 Feb;7(2):229–240. doi: 10.1101/gad.7.2.229. [DOI] [PubMed] [Google Scholar]
  27. Kaufman T. C., Seeger M. A., Olsen G. Molecular and genetic organization of the antennapedia gene complex of Drosophila melanogaster. Adv Genet. 1990;27:309–362. doi: 10.1016/s0065-2660(08)60029-2. [DOI] [PubMed] [Google Scholar]
  28. Kuziora M. A., McGinnis W. Autoregulation of a Drosophila homeotic selector gene. Cell. 1988 Nov 4;55(3):477–485. doi: 10.1016/0092-8674(88)90034-7. [DOI] [PubMed] [Google Scholar]
  29. Lewis E. B. A gene complex controlling segmentation in Drosophila. Nature. 1978 Dec 7;276(5688):565–570. doi: 10.1038/276565a0. [DOI] [PubMed] [Google Scholar]
  30. Lewis R. A., Wakimoto B. T., Denell R. E., Kaufman T. C. Genetic Analysis of the Antennapedia Gene Complex (Ant-C) and Adjacent Chromosomal Regions of DROSOPHILA MELANOGASTER. II. Polytene Chromosome Segments 84A-84B1,2. Genetics. 1980 Jun;95(2):383–397. doi: 10.1093/genetics/95.2.383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Macias A., Casanova J., Morata G. Expression and regulation of the abd-A gene of Drosophila. Development. 1990 Dec;110(4):1197–1207. doi: 10.1242/dev.110.4.1197. [DOI] [PubMed] [Google Scholar]
  32. Mann R. S., Hogness D. S. Functional dissection of Ultrabithorax proteins in D. melanogaster. Cell. 1990 Feb 23;60(4):597–610. doi: 10.1016/0092-8674(90)90663-y. [DOI] [PubMed] [Google Scholar]
  33. McGinnis W., Krumlauf R. Homeobox genes and axial patterning. Cell. 1992 Jan 24;68(2):283–302. doi: 10.1016/0092-8674(92)90471-n. [DOI] [PubMed] [Google Scholar]
  34. Merrill V. K., Diederich R. J., Turner F. R., Kaufman T. C. A genetic and developmental analysis of mutations in labial, a gene necessary for proper head formation in Drosophila melanogaster. Dev Biol. 1989 Oct;135(2):376–391. doi: 10.1016/0012-1606(89)90187-5. [DOI] [PubMed] [Google Scholar]
  35. Morata G., Botas J., Kerridge S., Struhl G. Homeotic transformations of the abdominal segments of Drosophila caused by breaking or deleting a central portion of the bithorax complex. J Embryol Exp Morphol. 1983 Dec;78:319–341. [PubMed] [Google Scholar]
  36. Morata G., Ripoll P. Minutes: mutants of drosophila autonomously affecting cell division rate. Dev Biol. 1975 Feb;42(2):211–221. doi: 10.1016/0012-1606(75)90330-9. [DOI] [PubMed] [Google Scholar]
  37. Reuter R., Panganiban G. E., Hoffmann F. M., Scott M. P. Homeotic genes regulate the spatial expression of putative growth factors in the visceral mesoderm of Drosophila embryos. Development. 1990 Dec;110(4):1031–1040. doi: 10.1242/dev.110.4.1031. [DOI] [PubMed] [Google Scholar]
  38. Simeone A., Gulisano M., Acampora D., Stornaiuolo A., Rambaldi M., Boncinelli E. Two vertebrate homeobox genes related to the Drosophila empty spiracles gene are expressed in the embryonic cerebral cortex. EMBO J. 1992 Jul;11(7):2541–2550. doi: 10.1002/j.1460-2075.1992.tb05319.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Simpson-Brose M., Treisman J., Desplan C. Synergy between the hunchback and bicoid morphogens is required for anterior patterning in Drosophila. Cell. 1994 Sep 9;78(5):855–865. doi: 10.1016/s0092-8674(94)90622-x. [DOI] [PubMed] [Google Scholar]
  40. Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
  41. Struhl G. Genes controlling segmental specification in the Drosophila thorax. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7380–7384. doi: 10.1073/pnas.79.23.7380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Struhl G. Role of the esc+ gene product in ensuring the selective expression of segment-specific homeotic genes in Drosophila. J Embryol Exp Morphol. 1983 Aug;76:297–331. [PubMed] [Google Scholar]
  43. Sánchez-Herrero E., Guerrero I., Sampedro J., González-Reyes A. Developmental consequences of unrestricted expression of the abd-A gene of Drosophila. Mech Dev. 1994 Jun;46(3):153–167. doi: 10.1016/0925-4773(94)90068-x. [DOI] [PubMed] [Google Scholar]
  44. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
  45. Tremml G., Bienz M. Induction of labial expression in the Drosophila endoderm: response elements for dpp signalling and for autoregulation. Development. 1992 Oct;116(2):447–456. doi: 10.1242/dev.116.2.447. [DOI] [PubMed] [Google Scholar]
  46. Wakimoto B. T., Kaufman T. C. Analysis of larval segmentation in lethal genotypes associated with the antennapedia gene complex in Drosophila melanogaster. Dev Biol. 1981 Jan 15;81(1):51–64. doi: 10.1016/0012-1606(81)90347-x. [DOI] [PubMed] [Google Scholar]
  47. Walldorf U., Gehring W. J. Empty spiracles, a gap gene containing a homeobox involved in Drosophila head development. EMBO J. 1992 Jun;11(6):2247–2259. doi: 10.1002/j.1460-2075.1992.tb05284.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wang B. B., Müller-Immergluck M. M., Austin J., Robinson N. T., Chisholm A., Kenyon C. A homeotic gene cluster patterns the anteroposterior body axis of C. elegans. Cell. 1993 Jul 16;74(1):29–42. doi: 10.1016/0092-8674(93)90292-x. [DOI] [PubMed] [Google Scholar]
  49. Wedeen C., Harding K., Levine M. Spatial regulation of Antennapedia and bithorax gene expression by the Polycomb locus in Drosophila. Cell. 1986 Mar 14;44(5):739–748. doi: 10.1016/0092-8674(86)90840-8. [DOI] [PubMed] [Google Scholar]

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