Abstract
We have isolated three classes of “enhancertrap” lines of Drosophila in which lacZ expression patterns in the imaginal discs are consistent with the idea of a polar (radial and angular) coordinate system of positional information. In the first class (HZ76), a circular pattern was expressed transiently during the mid-third instar larval stage when the radial components of the coordinate are probably generated. The expression patterns of the second class (HZ84) were sector-shaped and circular in the leg disc, suggesting a correlation with both radial and angular coordinate values. The expression patterns found in the third class (PZ63 and PZ22) were circular and appeared to reflect radial positional values. Expression in the latter two classes always began in the presumptive dorsal region of the leg disc and gradually spread to the ventral region. These developmental profiles of expression suggested the existence of a centre that initiates patterned gene expression in the presumptive dorsal region of the leg disc. The PZ22 line showed transient expression during tarsal segmentation, suggesting its involvement in tarsal segment formation. We have cloned the PZ22 gene and partially determined its sequence. The deduced amino acid sequence contained a zinc finger motif found in DNA/RNA binding proteins. By in situ hybridization, we determined that the PZ22 gene was transcribed in the leg disc in a pattern identical to that of the lacZ expression. In addition, it was expressed transiently in the embryonic mesoderm during mesoderm segmentation. The PZ22 gene, therefore, may function both in mesodermal segmentation in the embryo and in tarsal segmentation in the imaginal disc.
Similar content being viewed by others
References
Akam M (1987) The molecular basis for metameric pattern in the Drosophila embryo. Development 101:1–22
Angel M, Kerridge S, Vola C, Griffin-Shea R (1989) Two transcripts from the rotund region of Drosophila show similar positional specificities in imaginal disc tissues. Genes Dev 3:85–95
Basler K, Struhl G (1994) Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368:208–214
Bellen HJ, O'Kane CJ, Wilson C, Grossniklaus U, Pearson RK, Gehring WJ (1989) P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev 3:1288–1300
Bender W, Spierer P, Hogness DS (1983) Chromosomal walking and jumping to isolate DNA from the ace and rosy loci and the bithorax complex in Drosophila melanogaster. J Mol Biol 168:17–33
Bier E, Vaessin H, Shepherd S, Lee K, McCall K, Barbel S, Ackerman L, Carretto R, Uemura T, Grell E, Jan LY, Jan YN (1989) Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev 3:1273–1287
Bourgouin C, Lundgren SE, Thomas JB (1992) apterous is a Drosophila LIM domain gene required for the development of a subset of embryonic muscles. Neuron 9:549–561
Bryant PJ (1975) Pattern formation in the imaginal wing disc of Drosophila melanogaster: fate map, regeneration and duplication. J Exp Zool 193:49–78
Bryant PJ (1993) The polar coordinate model goes molecular. Science 259:471–472
Bryant SV French V, Bryant PJ (1981) Distal regeneration and symmetry. Science 212:993–1002
Campos-Ortega JA, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Springer, Berlin Heidelberg New York
Cavener DR (1987) Comparison of consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucl Acids Res 15:1353–1361
Chan EKL, Hamel JC, Buyon JP, Tan EM (1991) Molecular definition and sequence motifs of the 52-kD component of human SS-A/Ro autoantigen. J Clin Invest 87:68–76
Cohen SM, Jurgens G (1989) Proximal-distal pattern formation in Drosophila: graded requirement for Distal-less gene activity during limb development. Roux's Arch Dev Biol 198:157–169
Cohen B, McGuffin ME, Pfeifle C, Segal D, Cohen SM (1992) apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. Genes Dev 6:715–729
Couso JP, Bate M, Martinez-Arias A (1993) A wingless-dependent polar coordinate system in Drosophila imaginal discs. Science 259:484–489
Engels WR, Preston CR, Thompson P, Eggleston WB (1986) In situ hybridization to Drosophila salivary chromosomes with biotinylated DNA probes and alkaline phosphatase. Focus 8:6–8
Ferguson EL, Anderson KV (1992) decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71:451–461
French V, Bryant PJ, Bryant SV (1976) Pattern regulation in epimorphic fields. Science 193:969–981
Frutos R, Kimura K, Peterson KR (1989) In situ hybridization of Drosophila polytene chromosomes with digoxigenin-dUTP labeled probes. Trends Genet 5:366
Fyrberg EA, Mahaffey JW Bond BJ, Davidson N (1983) Transcripts of the six Drosophila actin genes accumulate in a stage- and tissue-specific manner. Cell 33:115–123
Ghysen A, O'Kane C (1989) Neural enhancer-like elements as specific cell markers in Drosophila. Development 105:35–52
Held LI Jr, Heup MA, Sappington JM, Peters SD (1994) Interactions of decapentaplegic, wingless, and Distal-less in the Drosophila leg. Roux's Arch Dev Biol 203:310–319
Hooper JE (1986) Homeotic gene function in the muscles of Drosophila larvae. EMBO J 5:2321–2329
Jowett T (1986) Preparation of nucleic acids. In: Roberts DB (ed) A practical approach. IRL Press, Oxford Washington DC, pp 275–286
Leiss D, Hinz U, Gasch A, Mertz R, Renkawitz-Pohl R (1988) 33 tubulin expression characterizes the differentiating mesodermal germ layer during Drosophila embryogenesis. Development 104:525–531
Masucci JD, Miltenberger RJ, Hoffmann FM (1990) Pattern-specific expression of the Drosophila decapentaplegic gene in imaginal disks is regulated by 3′ cis-regulatory element. Genes Dev 4:2011–2023
Mlodzik M, Hiromi Y (1992) The enhancer trap method in Drosophila: its application to neurobiology. Meth Neurosci 9:397–414
Murakami R, Shigenaga A, Kawano E, Matsumoto A, Yamaoka I, Tanimura T (1994) Novel tissue units of regional differentiation in the gut epithelium of Drosophila, as revealed by P-element-mediated detection of enhancer. Roux's Arch Dev Biol 203:243–249
O'Kane CJ, Gehring WJ (1987) Detection in situ of genomic regulatory elements in Drosophila. Proc Natl Acad Sci USA 84:9123–9127
Patarca R, Schwartz J, Singh RP, Kong QT, Murphy E, Anderson Y, Sheng FYW Singh P, Johnson KA, Guarnagia SM, Durfee T, Blattner F, Cantor H (1988) rpt-1, an intracellular protein from helper/inducer T cells that regulates gene expression of interleukin 2 receptor and human immunodeficiency virus type 1. Proc Natl Acad Sci USA 85:2733–2737
Phillips RG, Roberts IJH, Ingham PW Whittle RS (1990) The Drosophila segment polarity gene patched is involved in a position-signalling mechanism in imaginal discs. Development 110:105–114
Raftery LA, Sanicola M, Blackman RK, Gelbart WM (1991) The relationship of decapentaplegic and engrailed expression in Drosophila imaginal disks: do these genes mark the anteriorposterior compartment boundary? Development 113:27–33
Reddy BA, Etkin LD, Freemont PS (1992) A novel zinc finger coiled-coil domain in a family of nuclear proteins. Trends Biol Sci 17:344–345
Reddy BA, Kloc M, Etkin L (1991) The cloning and characterization of a maternally expressed novel zinc finger nuclear phosphoprotein (xnf7) in Xenopus laevis. Dev Biol 148:107–116
Robertson HM, Preston CR, Phillis RW, Johnson-Schlitz D, Benz WK, Engels WR (1988) A stable source of P-element transposase in Drosophila melanogaster. Genetics 118:461–470
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual. 2nd edn. Cold Spring Harbor Lab., Cold Spring Harbor, New York
Schubiger G (1968) Anlageplan, Determinationszustand und Transdeterminationsleistungen der männlichen Vorderbeinscheibe von Drosophila melanogaster. Wilhelm Roux's Arch Entwicklungsmech Org 160:9–40
Spencer FA, Hoffmann FM, Gelbart WM (1982) Decapentaplegic: A gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28:451–461
Strub S (1977) Developmental potentials of the cells of the male foreleg disc of Drosophila. I. Pattern regulation in insect fragments. Roux's Arch Dev Biol 181:309–320
Struhl G, Basler K (1993) Organizing activity of wingless protein in Drosophila. Cell 72:527–540
Takahashi M, Inaguma Y, Hiai H, Hirose F (1988) Developmentally regulated expression of a human “finger”-containing gene encoded by the 5′ half of the ret transforming gene. Mol Cell Biol 8:1853–1856
Tautz D, Pfeifle C (1989) A nonradioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of segmentation gene hunchback. Chromosoma 98:81–85
Wilson C, Pearson RK, Bellen HJ, O'Kane CJ, Grossniklaus U, Gehring WJ (1989) P-element-mediated enhancer detection: an efficient method for isolating and characterizing developmentally regulated genes in Drosophila. Genes Dev 3:1301–1313
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Goto, S., Tanimura, T. & Hotta, Y. Enhancer-trap detection of expression patterns corresponding to the polar coordinate system in the imaginal discs of Drosophila melanogaster . Roux's Arch Dev Biol 204, 378–391 (1995). https://doi.org/10.1007/BF00360483
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00360483