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. 1996 Aug 6;93(16):8479–8484. doi: 10.1073/pnas.93.16.8479

Class 3 Hox genes in insects and the origin of zen.

F Falciani 1, B Hausdorf 1, R Schröder 1, M Akam 1, D Tautz 1, R Denell 1, S Brown 1
PMCID: PMC38697  PMID: 8710895

Abstract

We have cloned, from a beetle and a locust, genes that are homologous to the class 3 Hox genes of vertebrates. Outside the homeobox they share sequence motifs with the Drosophila zerknüllt (zen) and z2 genes, and like zen, are expressed only in extraembryonic membranes. We conclude that the zen genes of Drosophila derive from a Hox class 3 sequence that formed part of the common ancestral Hox cluster, but that in insects this (Hox) gene has lost its role in patterning the anterio-posterior axis of the embryo, and acquired a new function. In the lineage leading to Drosophila, the zen genes have diverged particularly rapidly.

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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. Averof M., Akam M. HOM/Hox genes of Artemia: implications for the origin of insect and crustacean body plans. Curr Biol. 1993 Feb;3(2):73–78. doi: 10.1016/0960-9822(93)90158-k. [DOI] [PubMed] [Google Scholar]
  3. Brown S. J., Hilgenfeld R. B., Denell R. E. The beetle Tribolium castaneum has a fushi tarazu homolog expressed in stripes during segmentation. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12922–12926. doi: 10.1073/pnas.91.26.12922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cai H., Kiefel P., Yee J., Duncan I. A yeast artificial chromosome clone map of the Drosophila genome. Genetics. 1994 Apr;136(4):1385–1399. doi: 10.1093/genetics/136.4.1385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dawes R., Dawson I., Falciani F., Tear G., Akam M. Dax, a locust Hox gene related to fushi-tarazu but showing no pair-rule expression. Development. 1994 Jun;120(6):1561–1572. doi: 10.1242/dev.120.6.1561. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Gehring W. J., Qian Y. Q., Billeter M., Furukubo-Tokunaga K., Schier A. F., Resendez-Perez D., Affolter M., Otting G., Wüthrich K. Homeodomain-DNA recognition. Cell. 1994 Jul 29;78(2):211–223. doi: 10.1016/0092-8674(94)90292-5. [DOI] [PubMed] [Google Scholar]
  8. González-Crespo S., Morata G. Control of Drosophila adult pattern by extradenticle. Development. 1995 Jul;121(7):2117–2125. doi: 10.1242/dev.121.7.2117. [DOI] [PubMed] [Google Scholar]
  9. Henikoff S. Gene silencing in Drosophila. Curr Top Microbiol Immunol. 1995;197:193–208. doi: 10.1007/978-3-642-79145-1_13. [DOI] [PubMed] [Google Scholar]
  10. Holland P. W., Holland L. Z., Williams N. A., Holland N. D. An amphioxus homeobox gene: sequence conservation, spatial expression during development and insights into vertebrate evolution. Development. 1992 Nov;116(3):653–661. doi: 10.1242/dev.116.3.653. [DOI] [PubMed] [Google Scholar]
  11. Kapoun A. M., Kaufman T. C. A functional analysis of 5', intronic and promoter regions of the homeotic gene proboscipedia in Drosophila melanogaster. Development. 1995 Jul;121(7):2127–2141. doi: 10.1242/dev.121.7.2127. [DOI] [PubMed] [Google Scholar]
  12. Kappen C., Schughart K., Ruddle F. H. Early evolutionary origin of major homeodomain sequence classes. Genomics. 1993 Oct;18(1):54–70. doi: 10.1006/geno.1993.1426. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Krumlauf R. Evolution of the vertebrate Hox homeobox genes. Bioessays. 1992 Apr;14(4):245–252. doi: 10.1002/bies.950140408. [DOI] [PubMed] [Google Scholar]
  15. Lemaire P., Garrett N., Kato K., Gurdon J. B. Construction of subtracted cDNA libraries enriched for cDNAs for genes expressed in the mesoderm of early Xenopus gastrulae. C R Acad Sci III. 1993 Sep;316(9):931–944. [PubMed] [Google Scholar]
  16. Maggert K., Levine M., Frasch M. The somatic-visceral subdivision of the embryonic mesoderm is initiated by dorsal gradient thresholds in Drosophila. Development. 1995 Jul;121(7):2107–2116. doi: 10.1242/dev.121.7.2107. [DOI] [PubMed] [Google Scholar]
  17. Manak J. R., Scott M. P. A class act: conservation of homeodomain protein functions. Dev Suppl. 1994:61–77. [PubMed] [Google Scholar]
  18. 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]
  19. Means A. L., Gudas L. J. The roles of retinoids in vertebrate development. Annu Rev Biochem. 1995;64:201–233. doi: 10.1146/annurev.bi.64.070195.001221. [DOI] [PubMed] [Google Scholar]
  20. Rushlow C., Frasch M., Doyle H., Levine M. Maternal regulation of zerknüllt: a homoeobox gene controlling differentiation of dorsal tissues in Drosophila. Nature. 1987 Dec 10;330(6148):583–586. doi: 10.1038/330583a0. [DOI] [PubMed] [Google Scholar]
  21. Rushlow C., Levine M. Role of the zerknüllt gene in dorsal-ventral pattern formation in Drosophila. Adv Genet. 1990;27:277–307. doi: 10.1016/s0065-2660(08)60028-0. [DOI] [PubMed] [Google Scholar]
  22. Rushton E., Drysdale R., Abmayr S. M., Michelson A. M., Bate M. Mutations in a novel gene, myoblast city, provide evidence in support of the founder cell hypothesis for Drosophila muscle development. Development. 1995 Jul;121(7):1979–1988. doi: 10.1242/dev.121.7.1979. [DOI] [PubMed] [Google Scholar]
  23. Singh G., Kaur S., Stock J. L., Jenkins N. A., Gilbert D. J., Copeland N. G., Potter S. S. Identification of 10 murine homeobox genes. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10706–10710. doi: 10.1073/pnas.88.23.10706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Slack J. M., Holland P. W., Graham C. F. The zootype and the phylotypic stage. Nature. 1993 Feb 11;361(6412):490–492. doi: 10.1038/361490a0. [DOI] [PubMed] [Google Scholar]
  25. St Johnston D., Driever W., Berleth T., Richstein S., Nüsslein-Volhard C. Multiple steps in the localization of bicoid RNA to the anterior pole of the Drosophila oocyte. Development. 1989;107 (Suppl):13–19. doi: 10.1242/dev.107.Supplement.13. [DOI] [PubMed] [Google Scholar]
  26. Stuart J. J., Brown S. J., Beeman R. W., Denell R. E. A deficiency of the homeotic complex of the beetle Tribolium. Nature. 1991 Mar 7;350(6313):72–74. doi: 10.1038/350072a0. [DOI] [PubMed] [Google Scholar]
  27. Valerius M. T., Li H., Stock J. L., Weinstein M., Kaur S., Singh G., Potter S. S. Gsh-1: a novel murine homeobox gene expressed in the central nervous system. Dev Dyn. 1995 Jul;203(3):337–351. doi: 10.1002/aja.1002030306. [DOI] [PubMed] [Google Scholar]
  28. van den Heuvel M., Harryman-Samos C., Klingensmith J., Perrimon N., Nusse R. Mutations in the segment polarity genes wingless and porcupine impair secretion of the wingless protein. EMBO J. 1993 Dec 15;12(13):5293–5302. doi: 10.1002/j.1460-2075.1993.tb06225.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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