Evidence for a composite anterior determinant in the hover fly Episyrphus balteatus (Syrphidae), a cyclorrhaphan fly with an anterodorsal serosa anlage

Development

Volumn 136, Issue 1, 2009, Pages 117-127

  Lemke, Steffen ^a   Schmidt Ott, Urs ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Bicoid; Developmental constraint; Episyrphus; Evolutionary development (EvoDevo); Fate map

Indexed keywords

BICOID PROTEIN; HUNCHBACK PROTEIN; INSECT PROTEIN; MESSENGER RNA; ORTHODENTICLE PROTEIN; UNCLASSIFIED DRUG;

ANTERIOR POSTERIOR AXIS; ARTICLE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO AXIS; EMBRYO PATTERN FORMATION; EMBRYO POLARITY; EPISYRPHUS BALTEATUS; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; FLY; GENE OVEREXPRESSION; GENETIC REGULATION; NONHUMAN; PHYLOGENY; PRIMORDIUM; PRIORITY JOURNAL; RNA INTERFERENCE; ANIMAL; ANIMAL EMBRYO; BIOLOGICAL MODEL; CYTOLOGY; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENETICS; INTEGUMENT; LARVA; METABOLISM; MOLECULAR GENETICS; MORPHOGENESIS; NUCLEOTIDE SEQUENCE; PRENATAL DEVELOPMENT; SEROSA;

EPISYRPHUS; EPISYRPHUS BALTEATUS; HEXAPODA; SYRPHIDAE;

ANIMALS; BASE SEQUENCE; BODY PATTERNING; DIPTERA; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSECT PROTEINS; INTEGUMENTARY SYSTEM; LARVA; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, MESSENGER; SEROUS MEMBRANE;

EID: 60749110468     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.030270     Document Type: Article

References (75)

1. Amaya, E., Musci, T. J. and Kirschner, M. W. (1991). Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos. Cell 66, 257-270.
2. Berman, B. P., Nibu, Y. D., P. B., Tomancak, P., Celniker, S. E., Levine, M., Rubin, G. M. and Eisen, M. B. (2002). Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc. Natl. Acad. Sci. USA 99, 757-762.
3. Brent, A., Yucel, G., Small, S. and Desplan, C. (2007). Permissive and instructive anterior patterning rely on mRNA localization in the wasp embryo. Science 315, 1841-1843.
4. Brown, S., Fellers, J., Shippy, T., Denell, R., Stauber, M. and Schmidt-Ott, U. (2001). A strategy for mapping bicoid on the phylogenetic tree. Curr. Biol. 11, R43-R44.
5. Bullock, S. L., Stauber, M., Prell, A., Hughes, J. R., Ish-Horowicz, D. and Schmidt-Ott, U. (2004). Differential cytoplasmic mRNA localization adjusts pair-rule transcription factor activity to cytoarchitecture in dipteran evolution. Development 131, 4251-4261.
6. Cho, P. F., Poulin, F., Andrew Cho-Park, Y. A., Cho-Park, I. B., Chicoine, J. D., Lasko, P. and Sonenberg, N. (2005). A new paradigm for translational control: inhibition via 50-30 mRNA tethering by Bicoid and the eIF4E cognate 4EHP. Cell 121, 411-423.
7. Collins, K. P. and Wiegmann, B. M. (2002). Phylogenetic relationships of the lower Cyclorrhapha (Diptera: Brachycera) based on 28S rDNA sequences. Insect Syst. Evol. 33, 445-456.
8. Copf, T., Schröder, R. and Averof, M. (2004). Ancestral role of caudal genes in axis elongation and segmentation. Proc. Natl. Acad. Sci. USA 101, 17711-17716.
9. Davis, G. and Patel, N. (2002). Short, long, and beyond: molecular and embryological approaches to insect segmentation. Annu. Rev. Entomol. 47, 669-699.
10. Driever, W. and Nüsslein-Volhard, C. (1988a). The Bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54, 95-104.
11. Driever, W. and Nüsslein-Volhard, C. (1988b). A gradient of bicoid protein in Drosophila embryos. Cell 54, 83-93.
12. Driever, W. and Nüsslein-Volhard, C. (1989). The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. Nature 337, 138-143.
13. Driever, W., Siegel, V. and Nüsslein-Volhard, C. (1990). Autonomous determination of anterior structures in the early Drosophila embryo by the bicoid morphogen. Development 109, 811-820.
14. Falciani, F., Hausdorf, B., Schröder, 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. USA 93, 8479-8484.
15. Finkelstein, R. and Perrimon, N. (1990). The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature 346, 485-488.
16. Gamberi, C., Peterson, D. S., He, L. and Gottlieb, E. (2002). An anterior function for the Drosophila posterior determinant Pumilio. Development 129, 2699-2710.
17. Gao, Q. and Finkelstein, R. (1998). Targeting gene expression to the head: the Drosophila orthodenticle gene is a direct target of the Bicoid morphogen. Development 125, 4185-4193.
18. Gao, Q., Wang, Y. and Finkelstein, R. (1996). Orthodenticle regulation during embryonic head development in Drosophila. Mech. Dev. 56, 3-15.
19. Gavis, E. R. and Lehmann, R. (1992). Localization of nanos RNA controls embryonic polarity. Cell 71, 301-313.
20. Goltsev, Y., Hsiong, W., Lanzaro, G. and Levine, M. (2004). Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos. Dev. Biol. 275, 435-446.
21. Grimaldi, D. and Engel, M. S. (2005). Evolution of Insects. Cambridge: Cambridge University Press.
22. Hartenstein, V. (1993). Atlas of Drosophila Development. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
23. Hülskamp, M., Schroeder, C., Pfeifle, C., Jaeckle, H. and Tautz, D. (1989). Posterior segmentation of the Drosophila embryo in the absence of a maternal posterior organizer gene. Nature 338, 629-632.
24. Hülskamp, M., Pfeifle, C. and Tautz, D. (1990). A morphogenetic gradient of Hunchback protein organizes the expression of the gap genes Krüppel and knirps in the early Drosophila embryo. Nature 346, 577-580.
25. Irish, V., Lehmann, R. and Akam, M. (1989). The Drosophila posterior-group gene nanos functions by repressing hunchback activity. Nature 338, 646-648.
26. Kosman, D., Mizutani, C. M., Lemons, D., Cox, W. G., McGinnis, W. and Bier, E. (2004). Multiplex detection of RNA expression in Drosophila embryos. Science 305, 846.
27. Lemke, S. J., Stauber, M., Shaw, P. J., Rafiqi, A. M., Prell, A. and Schmidt-Ott, U. (2008). bicoid occurrence and Bicoid-dependent hunchback regulation in lower cyclorrhaphan flies. Evol. Dev. 10, 413-420.
28. Lynch, J. A., Olesnicky, E. C. and Desplan, C. (2006). Regulation and function of tailless in the long germ wasp Nasonia vitripennis. Dev. Genes Evol. 216, 493-498.
29. Macdonald, P. M. and Struhl, G. (1986). A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature 324, 537-545.
30. Mlodzik, M., Gibson, G. and Gehring, W. J. (1990). Effects of ectopic expression of caudal during Drosophila development. Development 109, 271-277.
31. Moulton, J. K. and Wiegmann, B. M. (2004). Evolution and phylogenetic utility of CAD (rudimentary) among Mesozoic-aged Eremoneuran Diptera (Insecta). Mol. Phylogenet. Evol. 31, 363-378.
32. Murata, Y. and Wharton, R. P. (1995). Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80, 747-756.
33. Negre, B., Casillas, S., Suzanne, M., Sanchez-Herrero, E., Akam, M., Nefedov, M., Barbadilla, A., de Jong, P. and Ruiz, A. (2005). Conservation of regulatory sequences and gene expression patterns in the disintegrating Drosophila Hox gene complex. Genome Res. 15, 692-700.
34. Niessing, D., Dostatni, N., Jäckle, H. and Rivera-Pomar, R. (1999). Sequence interval within the PEST domain of Bicoid is important for translational repression of caudal mRNA in the anterior region of the Drosophila embryo. EMBO J. 18, 1966-1973.
35. Niessing, D., Driever, W., Sprenger, F., Taubert, H., Jäckle, H. and Rivera-Pomar, R. (2000). Homeodomain position 54 specifies transcriptional versus translational control by Bicoid. Mol. Cell 5, 395-401.
36. Niessing, D., Blanke, S. and Jäckle, H. (2002). Bicoid associates with the 5′-cap-bound complex of caudal mRNA and represses translation. Genes Dev. 16, 2576-2582.
37. Ochoa-Espinosa, A., Yucel, G., Kaplan, L., Pare, A., Pura, N., Oberstein, A., Papatsenko, D. and Small, S. (2005). The role of binding site cluster strength in Bicoid-dependent patterning in Drosophila. Proc. Natl. Acad. Sci. USA 102, 4960-4965.
38. Olesnicky, E. C., Brent, A. E., Tonnes, L., Walker, M., Pultz, M. A., Leaf, D. and Desplan, C. (2006). A caudal mRNA gradient controls posterior development in the wasp Nasonia. Development 133, 3973-3982.
39. Patel, N. H., Martin-Blanco, E., Coleman, K. G., Poole, S. J., Ellis, M. C., Kornberg, T. B. and Goodman, C. S. (1989). Expression of engrailed proteins in arthropods, annelids and chordates. Cell 58, 955-968.
40. Posada, D. and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817-818.
41. Pultz, M. A., Pitt, J. N. and Alto, N. M. (1999). Extensive zygotic control of the anteroposterior axis in the wasp Nasonia vitripennis. Development 126, 701-710.
42. Pultz, M. A., Westendorf, L., Gale, S. D., Hawkins, K., Lynch, J., Pitt, J. N., Reeves, N. L., Yao, J. C. Y., Small, S., Desplan, C. et al. (2005b). A major role for zygotic hunchback in patterning the Nasonia embryo. Development 132, 3705-3715.
43. Rafiqi, A. M., Lemke, S. J., Ferguson, S., Stauber, M. and Schmidt-Ott, U. (2008). Evolutionary origin of the amnioserosa in cyclorrhaphan flies correlates with spatial and temporal expression changes of zen. Proc. Natl. Acad. Sci. USA 105, 234-239.
44. Rohr, K. B., Tautz, D. and Sander, K. (1999). Segmentation gene expression in the mothmidge Clogmia albipunctata (Diptera, Psychodidae) and other primitive dipterans. Dev. Genes Evol. 209, 145-154.
45. Roth, S. (2004). Gastrulation in other insects. In Gastrulation (ed. C. D. Stern), pp. 105-121. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
46. Schmidt-Ott, U. (2005). Insect serosa: a headline in comparative developmental genetics. Curr. Biol. 15, R245-R247.
47. Schmidt-Ott, U. and Technau, G. M. (1992). Expression of en and wg in the embryonic head and brain of Drosophila indicates a refolded band of seven segment remnants. Development 116, 111-125.
48. Schmidt-Ott, U., Sander, K. and Technau, G. M. (1994). Expression of engrailed in embryos of a beetle and five dipteran species with special reference to the terminal regions. Roux's Arch. Dev. Biol. 203, 298-303.
49. Schröder, R. (2003). The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 422, 621-625.
50. Schroeder, M. D., Pearce, M., Fak, J., Fan, H.-Q., Unnerstall, U., Emberly, E., Rajewsky, N., Siggia, E. D. and Gaul, U. (2004). Transcriptional control in the segmentation gene network of Drosophila. PLOS 2, e271.
51. Schulz, C., Schröder, R., Hausdorf, B., Wolff, C. and Tautz, D. (1998). A caudal homologue in the short germ band beetle Tribolium shows similarities to both, the Drosophila and the vertebrate caudal expression patterns. Dev. Genes Evol. 208, 283-289.
52. Segal, E., Raveh-Sadka, T., Schroeder, M., Unnerstall, U. and Gaul, U. (2008). Predicting expression patterns from regulatory sequence in Drosophila segmentation. Nature 451, 535-540.
53. Shimodaira, H. and Hasegawa, M. (2001). CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17, 1246-1247.
54. Shinmyo, Y., Mito, T., Matsushita, T., Sarashina, I., Miyawaki, K., Ohuchi, H. and Noji, S. (2005). caudal is required for gnathal and thoracic patterning and for posterior elongation in the intermediate-germband cricket Gryllus bimaculatus. Mech. Dev. 122, 231-239.
55. Simpson-Brose, M., Treisman, J. and Desplan, C. (1994). Synergy between the hunchback and bicoid morphogens is required for anterior patterning in Drosophila. Cell 78, 855-865.
56. Sommer, R. and Tautz, D. (1991). Segmentation gene expression in the housefly Musca domestica. Development 113, 419-430.
57. Sonoda, J. and Wharton, R. P. (1999). Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev. 13, 2704-2712.
58. Sonoda, J. and Wharton, R. P. (2001). Drosophila Brain Tumor is a translational repressor. Genes Dev. 15, 762-773.
59. St Johnston, D. and Nüsslein-Volhard, C. (1992). The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201-220.
60. 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. USA 97, 10844-10849.
61. Stauber, M., Prell, A. and Schmidt-Ott, U. (2002). A single Hox3 gene with composite bicoid and zerknüllt expression characteristics in non-Cyclorrhaphan flies. Proc. Natl. Acad. Sci. USA 99, 274-279.
62. Stauber, M., Lemke, S. and Schmidt-Ott, U. (2008). Expression and regulation of caudal in the lower cyclorrhaphan fly Megaselia. Dev. Genes Evol. 218, 81-87.
63. Stern, D. L. and Sucena, E. (2000). Preparation of larval and adult cuticles for light microscopy. In Drosophila Protocols (ed. W. Sullivan, M. Ashburner and R. S. Hawley), pp. 601-615. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
64. Struhl, G. (1989). Differing strategies for organizing anterior and posterior body pattern in Drosophila embryos. Nature 338, 741-744.
65. Struhl, G., Struhl, K. and Macdonald, P. M. (1989). The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell 57, 1259-1273.
66. Surkova, S., Kosman, D., Kozlov, K., Manu Myasnikova, E., Samsonova, A. A., Spirov, A., Vanario-Alonso, C. E., Samsonova, M. and Reinitz, J. (2008). Characterization of the Drosophila segment determination morphome. Dev. Biol. 313, 844-862.
67. Swofford, D. L. (2002). PAUP* Phylogenetic analysis using parsimony (* and other methods). Sunderland, MA: Sinauer Associates.
68. Tautz, D. (1988). Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centers. Nature 332, 281-284.
69. Tautz, D. and Pfeifle, C. (1989). 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 98, 81-85.
70. Tautz, D., Lehmann, R., Schnürch, H., Schuh, R., Seifert, E., Kienlin, A., Jones, K. and Jackle, H. (1987). Finger protein of novel structure encoded by hunchback, a second member of the gap class of Drosophila segmentation genes. Nature 327, 383-389.
71. Tautz, D., Friedrich, M. and Schröder, R. (1994). Insect embryogenesis: what is ancestral and what is derived? Development Suppl. 193-199.
72. Vardy, L. and Orr-Weaver, T. L. (2007). Regulating translation of maternal messages: multiple repression mechanisms. Trends Cell Biol. 17, 547-554. Wharton, R. P. and Struhl, G. (1991). RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos. Cell 67, 955-968.
73. Wolff, C., Sommer, R., Schröder, R., Glaser, G. and Tautz, D. (1995). Conserved and divergent expression aspects of the Drosophila segmentation gene hunchback in the short germ band embryo of the flour beetle Tribolium. Development 121, 4227-4236.
74. Yeates, D. K. and Wiegmann, B. M. (2005). Phylogeny and evolution of Diptera: recent insights and new perspectives. In The evolutionary Biology of Flies (ed. D. K. Yeates and B. M. Wiegmann), pp. 14-44. New York: Columbia University Press.
75. Zdobnov, E. M., von Mering, C., Letunic, I., Torrents, D., Suyama, M., Copley, R. R., Christophides, G. K., Thomasova, D., Holt, R. A., Subramanian, G. M. et al. (2002). Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science 298, 149-159.