Abstract
In order to test for bicoid-like activity in insects other than Drosophila melanogaster, anterior egg cytoplasm from the following species was injected into cleavage stage embryos from mutant D. melanogaster lacking a functional bicoid (bcd) product: six other Drosophila species, the housefly, three blowfly species, the primitive cyclorrhaphic dipteran Megaselia, and the honeybee Apis mellifera; preliminary tests were made with four lower dipterans (Nematocera). Rescue effects were only observed with the drosophilids, housefly, and two of the three blowfly species. Rescue was stronger with the drosophilids than with the other flies as donors. Where checked (D. pseudoobscura), a positive correlation was found between the amount of cytoplasm injected and the number of pattern elements formed, suggesting threshold effects upon target genes as with the endogenous bcd product. By polymerase chain reaction, fragments from a bcd-orthologous homeobox were cloned from the three blowfly species. The derived sequence of 43 amino acids was identical in all blowflies and the housefly but differed at 4 positions from the orthologous D. melanogaster sequence. Localization of the mRNA recognized by the respective fragments in the blowflies Lucilia and Phormia resembled that known from D. melanogaster, while Calliphora — the blowfly species lacking rescue activity —showed remarkable differences of localization in both ovarian follicles and the deposited egg cell. This surprising divergence within a morphologically rather uniform family of cyclorrhaphic dipterans should be of interest from both functional and evolutionary points of view.
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References
Becker T, Technau GM (1990) Single cell transplantation reveals interspecific cell communication in Drosophila chimeras. Development 109:821–832
Berleth T, Burri M, Thoma G, Bopp D, Richstein S, Frigerio G, Noll M, Nüsslein-Volhard C (1988) The role of localization of bicoid RNA in the anterior pattern of the Drosophila embryo. EMBO J 7:1749–1756
Beverley SM, Wilson AC (1984) Molecular evolution in Drosophila and the Higher Diptera. II. A time scale for fly evolution. J Mol Evol 21:1–13
Bohrmann J, Kiefer G, Sander K (1986) Inverse correlation between mean nuclear DNA content and cell number in nurse cell clusters of Drosophila. Chromosoma 94:36–44
Cohen S, Jürgens G (1991) Drosophila headlines. Trends Genet 7:267–272
Driever W, Nüsslein-Volhard C (1988) A gradient of bicoid protein in Drosophila embryos. Cell 54:83–93
Driever W, Thoma G, Nüsslein-Volhard C (1989) Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen. Nature 340:363–367
Driever W, Siegel V, Nüsslein-Volhard C (1990) Autonomous determination of anterior structures in the early Drosophila embryo by the bicoid morphogen. Development 109:811–820
Fitch WM (1970) Distinguishing homologous from analogous proteins. Syst Zool 19:99–113
Fleig R, Sander K (1986) Embryogenesis of the honeybee Apis mellifera L. (Hymenoptera, Apidae): an SEM study. Int J Insect Morphol Embryol 15:449–462
Frigerio G, Burri M, Bopp D, Baumgartner S, Noll M (1986) Structure of the segmentation gene paired and the Drosophila PRD gene set as part of a gene network. Cell 47:735–746
Frohnhöfer HG, Nüsslein-Volhard C (1986) Organisation of anterior pattern in the Drosophila embryo by the maternal gene bicoid. Nature 324:120–125
Frohnhöfer HG, Lehmann R, Nüsslein-Volhard C (1986) Manipulating the anteroposterior pattern of the Drosophila embryo. J Embryol Exp Morphol (Suppl) 97:169–179
Hanes SD, Brent R (1989) DNA specificity of the bicoid activator protein is determined by homeodomain recognition helix residue 9. Cell 57:1275–1283
Hülskamp M, Tautz D (1991) Gap genes and gradients — the logic behind the gaps. BioEssays 13:261–268
Lemeunier F, David JR, Tsacas L, Ashburner M (1986) The melanogaster species group. In: Ashburner M, Carson HL, Thompson JN (eds) The genetics and biology of Drosophila, vol 3c. Academic Press, New York, pp 148–256
Lindsley DL, Zimm GG (1992) The genome of Drosophila melanogaster. Academic Press, New York
McDonald PM, Struhl G (1986) A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature 324:437–445
Mitchison TJ, Sedat J (1983) Localization of antigenic determinants on whole Drosophila embryos. Dev Biol 99:261–264
Mohler J (1993) Genetic regulation of CNC expression in the pharyngeal primordia of Drosophila blastoderm embryos. Roux's Arch Dev Biol 202:214–223
Patel NH, Goodman CS (1992) DIG-labeled single-stranded DNA probes for in situ hybridisation. In: Kessler C (ed) Nonradioactive labeling and detection of biomolecules. Springer, Berlin Heidelberg New York, pp 377–381
Reuter D, Schuh R, Jäckle H (1989) The hometic gene spalt (sal) evolved during Drosophila speciation. Proc Natl Acad Sci USA 86:5483–5486
Sachs L (1978) Statistische Auswertungsmethoden, 5th edn. Springer Berlin Heidelberg New York
Saiki RK, Gelfand DH, Stoffel D, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Ehrlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
Sander K, Lehmann R (1988) Drosophila nurse cells produce a posterior signal required for embryonic segmentation and polarity. Nature 335:68–70
Santamaria P, Nüsslein-Volhard C (1983) Partial rescue of dorsal, a maternal effect mutation affecting the dorso-ventral pattern of the Drosophila embryo, by the injection of wild-type cytoplasm. EMBO J 2:1695–1699
Schröder R (1992) Mechanismen der frühembryonalen Musterbildung bei verschiedenen Insektenarten. PhD thesis, Albert-Ludwigs-Universität Freiburg
Seeger MA, Kaufman TC (1990) Molecular analysis of the bicoid gene from rosophila pseudoobscura: identification of conserved domains within coding and noncoding regions of the bicoid mRNA. EMBO J 9:2977–2987
Sommer R (1992) Vergleichende Analyse von Segmentierungsgenen bei Insekten. PhD thesis, Ludwig-Maximilians-Universität München
Sommer R, Tautz D (1991) Segmentation gene expression in the housefly Musca domestica. Development 113:419–430
Sommer R, Retzlaff M, Görlich K, Sander K, Tautz D (1992) Evolutionary conservation of zinc-finger domains of Drosophila segmentation genes. Proc Natl Acad Sci USA 89:10782–10786
StJohnston D, Nüsslein-Volhard C (1992) The origin of pattern and polarity in the Drosophila embryo. Cell 68:201–219
StJohnston D, Driever W, Berleth T, Richstein S, Nüsslein-Volhard C (1989) Multiple steps in the localization of bicoid RNA to the anterior pole of the Drosophila oocyte. Development (Suppl) 107:13–19
Struhl G, Struhl K, Macdonald PM (1989) The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell 57:1259–1273
Tautz D, (1988) Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres. Nature 332:281–284
Tautz D, Pfeifle C (1989) A non-radioactive in situ hybridisation method for the localisation of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98:81–85
Tautz D, Hülskamp M, Sommer RJ (1992) Whole mount in situ hybridisation in Drosophila. In: Wilkinson DG In situ hybridisation; a practical approach. IRL Press, Oxford, pp 61–73
Tearle R, Nüsslein-Volhard C (1987) Tübingen mutant stock list. Drosophila Inf Serv 66:209–269
Throckmorton LH (1975) The phylogeny, ecology and geography of Drosophila. In: King RC (ed) Handbook of genetics, vol 3. Plenum Press, New York, pp 421–469
Treier M, Pfeifle C, Tautz D (1989) Comparison of the gap segmentation gene hunchback between Drosophila melanogaster and Drosophila virilis reveals novel modes of evolutionary change. EMBO 8:1517–1525
Wieschaus E, Nüsslein-Volhard C (1986) Looking at embryos. In: Roberts DB (ed) Drosophila — a practical approach. IRL Press, Oxford, pp 199–227
Wyniger R (1974) Insektenzucht. Eugen Ulmer, Stuttgart
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Schröder, R., Sander, K. A comparison of transplantable bicoid activity and partial bicoid homeobox sequences in several Drosophila and blowfly species (Calliphoridae). Roux's Arch Dev Biol 203, 34–43 (1993). https://doi.org/10.1007/BF00539888
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DOI: https://doi.org/10.1007/BF00539888