The beetle Tribolium castaneum has a fushi tarazu homolog expressed in stripes during segmentation (original) (raw)

Abstract

The genetic control of embryonic organization is far better understood for the fruit fly Drosophila melanogaster than for any other metazoan. A gene hierarchy acts during oogenesis and embryogenesis to regulate the establishment of segmentation along the anterior-posterior axis, and homeotic selector genes define developmental commitments within each parasegmental unit delineated. One of the most intensively studied Drosophila segmentation genes is fushi tarazu (ftz), a pair-rule gene expressed in stripes that is important for the establishment of the parasegmental boundaries. Although ftz is flanked by homeotic selector genes conserved throughout the metazoa, there is no evidence that it was part of the ancestral homeotic complex, and it has been unclear when the gene arose and acquired a role in segmentation. We show here that the beetle Tribolium castaneum has a ftz homolog located in its Homeotic complex and expressed in a pair-rule fashion, albeit in a register differing from that of the fly gene. These and other observations demonstrate that a ftz gene preexisted the radiation of holometabolous insects and suggest that it has a role in beetle embryogenesis which differs somewhat from that described in flies.

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Selected References

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  1. Ananthan J., Baler R., Morrissey D., Zuo J., Lan Y., Weir M., Voellmy R. Synergistic activation of transcription is mediated by the N-terminal domain of Drosophila fushi tarazu homeoprotein and can occur without DNA binding by the protein. Mol Cell Biol. 1993 Mar;13(3):1599–1609. doi: 10.1128/mcb.13.3.1599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beeman R. W., Stuart J. J., Brown S. J., Denell R. E. Structure and function of the homeotic gene complex (HOM-C) in the beetle, Tribolium castaneum. Bioessays. 1993 Jul;15(7):439–444. doi: 10.1002/bies.950150702. [DOI] [PubMed] [Google Scholar]
  3. Beeman R. W., Stuart J. J., Haas M. S., Denell R. E. Genetic analysis of the homeotic gene complex (HOM-C) in the beetle Tribolium castaneum. Dev Biol. 1989 May;133(1):196–209. doi: 10.1016/0012-1606(89)90311-4. [DOI] [PubMed] [Google Scholar]
  4. Brown S. J., Patel N. H., Denell R. E. Embryonic expression of the single Tribolium engrailed homolog. Dev Genet. 1994;15(1):7–18. doi: 10.1002/dvg.1020150103. [DOI] [PubMed] [Google Scholar]
  5. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Doe C. Q., Hiromi Y., Gehring W. J., Goodman C. S. Expression and function of the segmentation gene fushi tarazu during Drosophila neurogenesis. Science. 1988 Jan 8;239(4836):170–175. doi: 10.1126/science.2892267. [DOI] [PubMed] [Google Scholar]
  8. Fitzpatrick V. D., Percival-Smith A., Ingles C. J., Krause H. M. Homeodomain-independent activity of the fushi tarazu polypeptide in Drosophila embryos. Nature. 1992 Apr 16;356(6370):610–612. doi: 10.1038/356610a0. [DOI] [PubMed] [Google Scholar]
  9. Frasch M., Warrior R., Tugwood J., Levine M. Molecular analysis of even-skipped mutants in Drosophila development. Genes Dev. 1988 Dec;2(12B):1824–1838. doi: 10.1101/gad.2.12b.1824. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Ingham P. W., Martinez Arias A. Boundaries and fields in early embryos. Cell. 1992 Jan 24;68(2):221–235. doi: 10.1016/0092-8674(92)90467-q. [DOI] [PubMed] [Google Scholar]
  12. Ingham P. W., Martinez-Arias A. The correct activation of Antennapedia and bithorax complex genes requires the fushi tarazu gene. Nature. 1986 Dec 11;324(6097):592–597. doi: 10.1038/324592a0. [DOI] [PubMed] [Google Scholar]
  13. Ish-Horowicz D., Pinchin S. M., Ingham P. W., Gyurkovics H. G. Autocatalytic ftz activation and metameric instability induced by ectopic ftz expression. Cell. 1989 Apr 21;57(2):223–232. doi: 10.1016/0092-8674(89)90960-4. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Lawrence P. A., Johnston P., Macdonald P., Struhl G. Borders of parasegments in Drosophila embryos are delimited by the fushi tarazu and even-skipped genes. 1987 Jul 30-Aug 5Nature. 328(6129):440–442. doi: 10.1038/328440a0. [DOI] [PubMed] [Google Scholar]
  16. Macdonald P. M., Ingham P., Struhl G. Isolation, structure, and expression of even-skipped: a second pair-rule gene of Drosophila containing a homeo box. Cell. 1986 Dec 5;47(5):721–734. doi: 10.1016/0092-8674(86)90515-5. [DOI] [PubMed] [Google Scholar]
  17. Maier D., Preiss A., Powell J. R. Regulation of the segmentation gene fushi tarazu has been functionally conserved in Drosophila. EMBO J. 1990 Dec;9(12):3957–3966. doi: 10.1002/j.1460-2075.1990.tb07616.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Manoukian A. S., Krause H. M. Concentration-dependent activities of the even-skipped protein in Drosophila embryos. Genes Dev. 1992 Sep;6(9):1740–1751. doi: 10.1101/gad.6.9.1740. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Müller J., Bienz M. Sharp anterior boundary of homeotic gene expression conferred by the fushi tarazu protein. EMBO J. 1992 Oct;11(10):3653–3661. doi: 10.1002/j.1460-2075.1992.tb05450.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nagy L. M., Carroll S. Conservation of wingless patterning functions in the short-germ embryos of Tribolium castaneum. Nature. 1994 Feb 3;367(6462):460–463. doi: 10.1038/367460a0. [DOI] [PubMed] [Google Scholar]
  22. Patel N. H., Ball E. E., Goodman C. S. Changing role of even-skipped during the evolution of insect pattern formation. Nature. 1992 May 28;357(6376):339–342. doi: 10.1038/357339a0. [DOI] [PubMed] [Google Scholar]
  23. Patel N. H., Condron B. G., Zinn K. Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles. Nature. 1994 Feb 3;367(6462):429–434. doi: 10.1038/367429a0. [DOI] [PubMed] [Google Scholar]
  24. Patel N. H., Kornberg T. B., Goodman C. S. Expression of engrailed during segmentation in grasshopper and crayfish. Development. 1989 Oct;107(2):201–212. doi: 10.1242/dev.107.2.201. [DOI] [PubMed] [Google Scholar]
  25. Scott M. P., Tamkun J. W., Hartzell G. W., 3rd The structure and function of the homeodomain. Biochim Biophys Acta. 1989 Jul 28;989(1):25–48. doi: 10.1016/0304-419x(89)90033-4. [DOI] [PubMed] [Google Scholar]
  26. Sommer R. J., Tautz D. Involvement of an orthologue of the Drosophila pair-rule gene hairy in segment formation of the short germ-band embryo of Tribolium (Coleoptera) Nature. 1993 Feb 4;361(6411):448–450. doi: 10.1038/361448a0. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Stuart J. J., Brown S. J., Beeman R. W., Denell R. E. The Tribolium homeotic gene Abdominal is homologous to abdominal-A of the Drosophila bithorax complex. Development. 1993 Jan;117(1):233–243. doi: 10.1242/dev.117.1.233. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. Walldorf U., Fleig R., Gehring W. J. Comparison of homeobox-containing genes of the honeybee and Drosophila. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9971–9975. doi: 10.1073/pnas.86.24.9971. [DOI] [PMC free article] [PubMed] [Google Scholar]