Patterns of conservation and change in honey bee developmental genes

Genome Research

Volumn 16, Issue 11, 2006, Pages 1376-1384

  Dearden, Peter K ^a   Wilson, Megan J ^a   Sablan, Lisha ^a   Osborne, Peter W ^a,f   Havler, Melanie ^a   McNaughton, Euan ^a   Kimura, Kiyoshi ^b   Milshina, Natalia V ^c   Hasselmann, Martin ^d   Gempe, Tanja ^d   Schioett, Morten ^d   Brown, Susan J ^e   Elsik, Christine G ^c   Holland, Peter W H ^f   Kadowaki, Tatsuhiko ^g   Beye, Martin ^d  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b NATIONAL INSTITUTE OF LIVESTOCK AND GRASSLAND SCIENCE   (Japan)

^c TEXAS A AND M UNIVERSITY   (United States)

^d HEINRICH HEINE UNIVERSITY   (Germany)

^e KANSAS STATE UNIVERSITY   (United States)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

LIM PROTEIN; TRANSCRIPTION FACTOR PAX2; TRANSCRIPTION FACTOR POU; WNT PROTEIN;

ARTICLE; CELL COMMUNICATION; DROSOPHILA; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; GENETIC VARIABILITY; HONEYBEE; HOX GENE; INSECT DEVELOPMENT; MEIOSIS; MOLECULAR EVOLUTION; ORTHOLOGY; PLEIOTROPY; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SEX DETERMINATION; SPECIES COMPARISON;

AMINO ACID SEQUENCE; ANIMALS; BEES; BODY PATTERNING; CONSERVED SEQUENCE; DOSAGE COMPENSATION, GENETIC; DROSOPHILA; EVOLUTION, MOLECULAR; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; GENES, INSECT; GERM CELLS; INSECT PROTEINS; MALE; MEIOSIS; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID; SEX DETERMINATION (GENETICS); SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

APIS MELLIFERA; HEXAPODA; INSECTA;

EID: 33750494971     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.5108606     Document Type: Article

References (79)

1. Adams, M.D., Celniker, S.E., Holt, R.A., Evans, C.A., Gocayne, J.D., Amanatides, P.G., Scherer, S.E., Li, P.W., Hoskins, R.A., Galle, R.F., et al. 2000. The genome sequence of Drosophila melanogaster. Science 287: 2185-2195.
2. Altschul, S., Gish, W., Miller, W., Myers, E., and Lipman, D. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
3. Amdam, G.V., Simoes, Z.L.P., Guidugli, K.R., Norberg, K., and Omholt, S.W. 2003. Disruption of vitellogenin gene function in adult honeybees by intra-abdominal injection of double stranded RNA. BMC Biotechnol. 3: 1.
4. Bachtrog, D. 2005. Sex chromosome evolution: Molecular aspects of Y-chromosome degeneration in Drosophila. Genome Res. 15: 1393-1401.
5. Baron, M. 2003. An overview of the Notch signalling pathway. Semin. Cell Dev. Biol. 14: 113-119.
6. Bejsovec, A. 2005. Wnt pathway activation: New relations and locations. Cell 120: 11-14.
7. Bergem, M., Norberg, K., and Aamodt, R.M. 2006. Long-term maintenance of in vitro cultured honeybee (Apis mellifera) embryonic cells. BMC Dev. Biol. 6: 17.
8. Beye, M., Hartel, S., Hagen, A., Hasselmann, M., and Omholt, S.W. 2002. Specific developmental gene silencing in the honey bee using a homeobox motif. Insect Mol. Biol. 11: 527-532.
9. Beye, M., Hasselmann, M., Fondrk, M.K., Page, R.E., and Omholt, S.W. 2003. The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114: 419-429.
10. Binner, P. and Sander, K. 1997. Pair-rule patterning in the honeybee Apis Mellifera; expression of even-skipped combines traits known from beetles and fruitfly. Dev. Genes Evol. 206: 447-454.
11. Brown, S.J., Fellers, J.P., Shippy, T.D., Richardson, E.A., Maxwell, M., Stuart, J.J., and Denell, R.E. 2002. Sequence of the Tribolium castaneum homeotic complex: The region corresponding to the Drosophila melanogaster antennapedia complex. Genetics 160: 1067-1074.
12. Casali, A. and Casanova, J. 2001. The spatial control of Torso RTK activation: A C-terminal fragment of the Trunk protein acts as a signal for Torso receptor in the Drosophila embryo. Development 128: 1709-1715.
13. Cline, T.W. and Meyer, B.J. 1996. Vive la difference: Males vs females in flies vs. worms. Annu. Rev. Genet. 30: 637-702.
14. Damen, W.G. 2002. Parasegmental organization of the spider embryo implies that the parasegment is an evolutionarily conserved entity in arthropod embryogenesis. Development 129: 1239-1250.
15. Davidson, E.H. 2001. Genomic regulatory systems. Academic Press, London.
16. Dearden, P.K. 2006. Germ cell development in the honeybee (Apis mellifera); vasa and nanos expression. BMC Dev. Biol. 6: 6.
17. Dearden, P., Grbic, M., Falciani, F., and Akam, M. 2000. Maternal expression and early zygotic expression of the Hox3/zen gene in Schistocerca. Evol. Dev. 2: 261-270.
18. Dearden, P., Donly, C., and Grbic, M. 2002. Expression of pair-rule gene homologues in a chelicerate: Early patterning of the Two-Spotted Spider Mite Tetranychus urticae. Development 129: 5461-5472.
19. Doyle, H.J., Kraut, R., and Levine, M. 1989. Spatial regulation of zerknullt: A dorsal-ventral patterning gene in Drosophila. Genes & Dev. 3: 1518-1533.
20. Drysdale, R.A. and Crosby, M.A. 2005. FlyBase: Genes and gene models. Nucleic Acids Res. 33: D390-D395.
21. Dubendorfer, A., Hediger, M., Burghardt, G., and Bopp, D. 2002. Musca domestica, a window on the evolution of sex-determining mechanisms in insects. Int. J. Dev. Biol. 46: 75-79.
22. DuPraw, E.J. 1967. The honeybee embryo. In Methods in developmental biology (eds. F.H. Wilt and N.K. Wessells), pp. 183-217. Thomas Y. Cromwell, New York.
23. Falciani, F., Hausdorf, B., Schroder, R., Akam, M., Tautz, D., Denell, R., and Brown, S. 1996. Class 3 Hox genes in insects and the origin of zen. Proc. Natl. Acad. Sci. 93: 8479-8484.
24. Felsenstein, J. 2004. PHYLIP (Phylogeny Inference Package) version 3.6. Department of Genomic Sciences, University of Washington, Seattle, WA.
25. Ferrier, D.E.K. and Akam, M. 1996. Organization of the Hox gene cluster in the grasshopper, Schistocerca gregaria. Proc. Natl. Acad. Sci. 93: 13024-13029.
26. Ferrier, D.E.K. and Holland, P.W.H. 2001. Sipunculan ParaHox genes. Evol. Dev. 3: 263-270.
27. Fleig, R. 1990. Engrailed expression and body segmentation in the honeybee, Apis mellifera. Rouxs Arch. Dev. Biol. 198: 467-473.
28. Fleig, R. and Sander, K. 1986. Embryogenesis of the honeybee Apis mellifera L. (Hymenoptera: Apidae): An SEM study. Int. J. Insect Morphol. Embryol. 15: 449-462.
29. Fleig, R., Walldorf, U., Gehring, W.J., and Sander, K. 1992. Development of the Deformed protein pattern in the embryo of the honeybee Apis mellifera L. (Hymenoptera). Rouxs Arch. Dev. Biol. 201: 235-242.
30. Furriols, M., Casali, A., and Casanova, J. 1998. Dissecting the mechanism of torso receptor activation. Mech. Dev. 70: 111-118.
31. Gay, N.J. and Keith, F.J. 1992. Regulation of translation and proteolysis during the development of embryonic dorso-ventral polarity in Drosophila. Homology of easter proteinase with Limulus proclotting enzyme and translational activation of Toll receptor synthesis. Biochim. Biophys. Acta 1132: 290-296.
32. Gonzalez-Gaitan, M., Rothe, M., Wimmer, E.A., Taubert, H., and Jackle, H. 1994. Redundant functions of the genes knirps and knirps-related for the establishment of anterior Drosophila head structures. Proc. Natl. Acad. Sci. 91: 8567-8571.
33. Hennig, W. 1981. Insect phylogeny. John Wiley, Bath, UK.
34. Holt, R.A., Subramanian, G.M., Halpern, A., Sutton, G.G., Charlab, R., Nusskern, D.R., Wincker, P., Clark, A.G., Ribeiro, J.M., Wides, R., et al. 2002. The genome sequence of the malaria mosquito Anopheles gambiae. Science 298: 129-149.
35. The Honey Bee Genome Sequencing Consortium. 2006. Insights into social insects from the genome of the honey bee Apis mellifera. Nature (in press).
36. Hooper, J.E. and Scott, M.P. 2005. Communicating with Hedgehogs Nat. Rev. Mol. Cell Biol. 6: 306-317.
37. Hughes, C.L. and Kaufman, T.C. 2002. Hox genes and the evolution of the arthropod body plan. Evol. Dev. 4: 459-499.
38. Jagla, K., Bellard, M., and Frasch, M. 2001. A cluster of Drosophila homeobox genes involved in mesoderm differentiation programs. Bioessays 23: 125-133.
39. Krauss, V., Pecyna, M., Kurz, K., and Sass, H. 2005. Phylogenetic mapping of intron positions: A case study of translation initiation factor eIF2γ. Mol. Biol. Evol. 22: 74-84.
40. Kusserow, A., Pang, K., Sturm, C., Hrouda, M., Lentfer, J., Schmidt, H.A., Technau, U., von Haeseler, A., Hobmayer, B., Martindale, M.Q., et al. 2005. Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433: 156-160.
41. Lehmann, R. and Nusslein-Volhard, C. 1986. Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila. Cell 47: 141-152.
42. Lewis, S.E., Searle, S.M., Harris, N., Gibson, M., Iyer, V., Richter, J., Wiel, C., Bayraktaroglir, L., Birney, E., Crosby, M.A., et al. 2002. Apollo: A sequence annotation editor. Genome Biol. 3: research0082.
43. Lewis, E.B., Pfeiffer, B.D., Mathog, D.R., and Celniker, S.E. 2003. Evolution of the homeobox complex in the Diptera. Curr. Biol. 13: R587-R588.
44. Liaw, G.J., Rudolph, K.M., Huang, J.D., Dubnicoff, T., Courey, A.J., and Lengyel, J.A. 1995. The torso response element binds GAGA and NTF-1/Elf-1, and regulates tailless by relief of repression. Genes & Dev. 9: 3163-3176.
45. Logan, C.Y. and Nusse, R. 2004. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20: 781-810.
46. Luke, G.N., Castro, L.F., McLay, K., Bird, C., Coulson, A., and Holland, P.W.H. 2003. Dispersal of NK homeobox gene clusters in amphioxus and humans. Proc. Natl. Acad. Sci. 100: 5292-5295.
47. MacDonald, P.M., Leask, A., and Kerr, K. 1995. exl protein specifically binds BLE1, a bicoid mRNA localization element, and is required for one phase of its activity. Proc. Natl. Acad. Sci. 92: 10787-10791.
48. Mahowald, A.P. 2001. Assembly of the Drosophila germ plasm. Int. Rev. Cytol. 203: 187-213.
49. Maxton Küchenmeister, J., Handel, K., Schmidt-Ott, U., Roth, S., and Jäckle, H. 1999. Toll homologue expression in the beetle Tribolium suggests a different mode of dorsoventral patterning than in Drosophila embryos. Mech. Dev. 83: 107-114.
50. Miller, D.J., Hayward, D.C., Reece-Hoyes, J.S., Scholten, I., Catmull, J., Gehring, W.J., Callaerts, P., Larsen, J.E., and Ball, E.E. 2000. Pax gene diversity in the basal cnidarian Acropora millepora (Cnidaria, Anthozoa): Implications for the evolution of the Pax gene family. Proc. Natl. Acad. Sci. 97: 4475-4480.
51. Nauber, U., Pankratz, M.J., Kienlin, A., Seifert, E., Klemm, U., and Jackle, H. 1988. Abdominal segmentation of the Drosophila embryo requires a hormone receptor-like protein encoded by the gap gene knirps. Nature 336: 489-492.
52. Nelson, J.A. 1915. The embryology of the honeybee. Princeton University Press, Princeton, NJ.
53. Nusse, R. 2001. An ancient cluster of Wnt paralogues. Trends Genet. 17: 443.
54. Osborne, P. and Dearden, P.K. 2005a. Expression of Pax group III genes in the honeybee (Apis mellifera). Dev. Genes Evol. 215: 499-508.
55. Osborne, P. and Dearden, P.K. 2005b. Non-radioactive in situ hybridisation to honeybees embryos and ovaries. Apidologie (Celle) 36: 113-118.
56. Pearson, J.C., Lemons, D., and McGinnis, W. 2005. Modulating Hox gene functions during animal body patterning. Nat. Rev. Genet. 6: 893-904.
57. Peel, A.D., Chipman, A.D., and Akam, M. 2005. Arthropod segmentation: Beyond the Drosophila paradigm. Nat. Rev. Genet. 6: 905-916.
58. Pires-daSilva, A. and Sommer, R.J. 2003. The evolution of signalling pathways in animal development. Nat. Rev. Genet. 4: 39-49.
59. Pultz, M.A., Westendorf, L., Gale, S.D., Hawkins, K., Lynch, J., Pitt, J.N., Reeves, N.L., Yao, J.C., Small, S., Desplan, C., et al. 2005. A major role for zygotic hunchback in patterning the Nasonia embryo. Development 132: 3705-3715.
60. Raftery, L.A. and Sutherland, D.J. 1999. TGF-β family signal transduction in Drosophila development: From Mad to Smads. Dev. Biol. 210: 251-268.
61. Ronquist, F. and Huelsenbeck, J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
62. Rothe, M., Nauber, U., and Jackle, H. 1989. Three hormone receptor-like Drosophila genes encode an identical DNA-binding finger. EMBO J. 8: 3087-3094.
63. Schlatter, R. and Maier, D. 2005. The Enhancer of split and Achaete-Scute complexes of Drosophilids derived from simple ur-complexes preserved in mosquito and honeybee. BMC Evol. Biol. 5: 67.
64. Schoppmeier, M. and Schroder, R. 2005. Maternal torso signaling controls body axis elongation in a short germ insect. Curr. Biol. 15: 2131-2136.
65. Schroder, R. 2003. The genes orthodenticle and hunchback substitute for bicoid in th beetle Tribolium. Nature 422: 621-625.
66. Schroder, R., Eckert, C., Wolff, C., and Tautz, D. 2000. Conserved and divergent aspects of terminal patterning in the beetle Tribolium castaneum. Proc. Natl. Acad. Sci. 97: 6591-6596.
67. Schüpbach, T. and Roth, S. 1994. Dorsoventral patterning in Drosophila oogenesis. Curr. Opin. Genet. Dev. 4: 502-507.
68. Schutt, C. and Nothiger, R. 2000. Structure, function and evolution of sex-determining systems in Dipteran insects. Development 127: 667-677.
69. Stauber, M., Jackle, H., and Schmidt-Ott, U. 1999. The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc. Natl. Acad. Sci. 96: 3786-3789.
70. Stauber, M., Taubert, H., and Schmidt-Ott, U. 2000. Function of bicoid and hunchback homologs in the basal cyclorrhaphan fly Megaselia (Phoridae). Proc. Natl. Acad. Sci. 97: 10844-10849.
71. Stauber, M., Prell, A., and Schmidt-Ott, U. 2002. A single Hox3 gene with composite bicoid and zerknullt expression characteristics in non-Cyclorrhaphan flies. Proc. Natl. Acad. Sci. 99: 274-279.
72. Thompson, J.D., Higgins, D.G., and Gibson, T.J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
73. van der Zee, M., Berns, N., and Roth, S. 2005. Distinct functions of the Tribolium zerknullt genes in serosa specification and dorsal closure. Curr. Biol. 15: 624-636.
74. Walldorf, U., Fleig, R., and Gehring, W.J. 1989. Comparison of homeobox-containing genes of the honeybee and Drosophila. Proc. Natl. Acad. Sci. 86: 9971-9975.
75. Walldorf, U., Binner, P., and Fleig, R. 2000. Hox genes in the honey bee Apis mellifera. Dev. Genes Evol. 210: 483-492.
76. Whiting, M.F. 2002. Phylogeny of the holometabolous insect orders: Molecular evidence. Zool. Scr. 31: 3-15.
77. Wilkins, A.S. 1995. Moving up the hierarchy: A hypothesis on the evolution of a genetic sex determination pathway. Bioessays 17: 71-77.
78. Wilkins, A.S. 2002. The evolution of developmental pathways. Sinauer Associates, Sunderland, MA.
79. Yasukochi, Y., Ashakumary, L.A., Wu, C., Yoshido, A., Nohata, J., Mita, K., and Sahara, K. 2004. Organization of the Hox gene cluster of the silkworm, Bombyx mori: A split of the Hox cluster in a non-Drosophila insect. Dev. Genes Evol. 214: 606-614.