Apparent role of Tribolium orthodenticle in anteroposterior blastoderm patterning largely reflects novel functions in dorsoventral axis formation and cell survival

Development

Volumn 137, Issue 11, 2010, Pages 1853-1862

  Kotkamp, Kay ^a,b   Klingler, Martin ^a   Schoppmeier, Michael ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Anteroposterior patterning; Bicoid; Dorsoventral patterning; Orthodenticle; Short germ insect; Tribolium

Indexed keywords

ANIMAL TISSUE; ARTICLE; BEETLE; BLASTODERM; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; GENE; MORPHOGENESIS; NONHUMAN; ORTHODENTICLE GENE; PRIORITY JOURNAL; RNA INTERFERENCE; TRIBOLIUM;

ANIMALS; BODY PATTERNING; CELL SURVIVAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; GENES, INSECT; PHENOTYPE; RNA INTERFERENCE; TRIBOLIUM;

COLEOPTERA; DIPTERA; HEXAPODA; TRIBOLIUM (BEETLE); TRIBOLIUM CASTANEUM;

EID: 77952161464     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.047043     Document Type: Article

References (72)

1. Adachi-Yamada, T. and O'Connor, M. B. (2002). Morphogenetic apoptosis: a mechanism for correcting discontinuities in morphogen gradients. Dev. Biol. 251, 74-90. (Pubitemid 35333748)
2. Ashe, H. L. and Levine, M. (1999). Local inhibition and long-range enhancement of Dpp signal transduction by Sog. Nature 398, 427-431.
3. Biehs, B., Francois, V. and Bier, E. (1996). The Drosophila short gastrulation gene prevents Dpp from autoactivating and suppressing neurogenesis in the neuroectoderm. Genes Dev. 10, 2922-2934. (Pubitemid 26394252)
4. Blankenship, J. T. and Wieschaus, E. (2001). Two new roles for the Drosophila AP patterning system in early morphogenesis. Development 128, 5129-5138. (Pubitemid 34083038)
5. Brent, A. E., 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.
6. 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.
7. Bucher, G. and Klingler, M. (2004). Divergent segmentation mechanism in the short germ insect Tribolium revealed by giant expression and function. Development 131, 1729-1740.
8. Bucher, G., Scholten, J. and Klingler, M. (2002). Parental RNAi in Tribolium (Coleoptera). Curr. Biol. 12, R85-R86.
9. Bucher, G., Farzana, L., Brown, S. J. and Klingler, M. (2005). Anterior localization of maternal mRNAs in a short germ insect lacking bicoid. Evol. Dev. 7, 142-149.
10. Carroll, S. B., Winslow, G. M., Twombly, V. J. and Scott, M. P. (1987). Genes that control dorsoventral polarity affect gene expression along the anteroposterior axis of the Drosophila embryo. Development 99, 327-332.
11. Cerny, A. C., Bucher, G., Schroder, R. and Klingler, M. (2005). Breakdown of abdominal patterning in the Tribolium Kruppel mutant jaws. Development 132, 5353-5363.
12. Cerny, A. C., Grossmann, D., Bucher, G. and Klingler, M. (2008). The Tribolium ortholog of knirps and knirps-related is crucial for head segmentation but plays a minor role during abdominal patterning. Dev. Biol. 321, 284-294.
13. Cho, P. F., Poulin, F., 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 5′-3′ mRNA tethering by Bicoid and the eIF4E cognate 4EHP. Cell 121, 411-423.
14. Choe, C. P., Miller, S. C. and Brown, S. J. (2006). A pair-rule gene circuit defines segments sequentially in the short-germ insect Tribolium castaneum. Proc. Natl. Acad. Sci. USA 103, 6560-6564.
15. Cohen, S. M. and Jurgens, G. (1990). Mediation of Drosophila head development by gap-like segmentation genes. Nature 346, 482-485.
16. Copf, T., Rabet, N., Celniker, S. E. and Averof, M. (2003). Posterior patterning genes and the identification of a unique body region in the brine shrimp Artemia franciscana. Development 130, 5915-5927.
17. DiNardo, S., Heemskerk, J., Dougan, S. and O'Farrell, P. H. (1994). The making of a maggot: patterning the Drosophila embryonic epidermis. Curr. Opin. Genet. Dev. 4, 529-534.
18. Driever, W. and Nusslein-Volhard, C. (1988). The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54, 95-104.
19. 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. USA 93, 8479-8484.
20. Finkelstein, R. and Perrimon, N. (1990). The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature 346, 485-488.
21. Finkelstein, R., Smouse, D., Capaci, T. M., Spradling, A. C. and Perrimon, N. (1990). The orthodenticle gene encodes a novel homeo domain protein involved in the development of the Drosophila nervous system and ocellar visual structures. Genes Dev. 4, 1516-1527.
22. 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.
23. Hader, T., La Rosee, A., Ziebold, U., Busch, M., Taubert, H., Jackle, H. and Rivera-Pomar, R. (1998). Activation of posterior pair-rule stripe expression in response to maternal caudal and zygotic knirps activities. Mech. Dev. 71, 177-186.
24. Hulskamp, M., Pfeifle, C. and Tautz, D. (1990). A morphogenetic gradient of hunchback protein organizes the expression of the gap genes Kruppel and knirps in the early Drosophila embryo. Nature 346, 577-580.
25. Klingensmith, J., Noll, E. and Perrimon, N. (1989). The segment polarity phenotype of Drosophila involves differential tendencies toward transformation and cell death. Dev. Biol. 134, 130-145.
26. Klingler, M. (2004). Tribolium. Curr. Biol. 14, R639-R640.
27. Kraut, R. and Levine, M. (1991). Spatial regulation of the gap gene giant during Drosophila development. Development 111, 601-609.
28. Lall, S. and Patel, N. H. (2001). Conservation and divergence in molecular mechanisms of axis formation. Annu. Rev. Genet. 35, 407-437.
29. Liaw, G. J. and Lengyel, J. A. (1993). Control of tailless expression by bicoid, dorsal and synergistically interacting terminal system regulatory elements. Mech. Dev. 40, 47-61.
30. Lynch, J. A., Brent, A. E., Leaf, D. S., Pultz, M. A. and Desplan, C. (2006). Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature 439, 728-732.
31. 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.
32. Magrassi, L. and Lawrence, P. A. (1988). The pattern of cell death in fushi tarazu, a segmentation gene of Drosophila. Development 104, 447-551.
33. Marques, G., Musacchio, M., Shimell, M. J., Wunnenberg-Stapleton, K., Cho, K. W. and O'Connor, M. B. (1997). Production of a DPP activity gradient in the early Drosophila embryo through the opposing actions of the SOG and TLD proteins. Cell 91, 417-426.
34. Marques-Souza, H., Aranda, M. and Tautz, D. (2008). Delimiting the conserved features of hunchback function for the trunk organization of insects. Development 135, 881-888.
35. Mlodzik, M., Gibson, G. and Gehring, W. J. (1990). Effects of ectopic expression of caudal during Drosophila development. Development 109, 271-277.
36. Moussian, B. and Roth, S. (2005). Dorsoventral axis formation in the Drosophila embryo-shaping and transducing a morphogen gradient. Curr. Biol. 15, R887-R899.
37. Namba, R., Pazdera, T. M., Cerrone, R. L. and Minden, J. S. (1997). Drosophila embryonic pattern repair: how embryos respond to bicoid dosage alteration. Development 124, 1393-1403.
38. Niessing, D., Dostatni, N., Jackle, H. and Rivera-Pomar, R. (1999). Sequence interval within the PEST motif of Bicoid is important for translational repression of caudal mRNA in the anterior region of the Drosophila embryo. EMBO J. 18, 1966-1973.
39. Niessing, D., Blanke, S. and Jackle, H. (2002). Bicoid associates with the 5′-capbound complex of caudal mRNA and represses translation. Genes Dev. 16, 2576-2582.
40. Nunes da Fonseca, R., von Levetzow, C., Kalscheuer, P., Basal, A., van der Zee, M. and Roth, S. (2008). Self-regulatory circuits in dorsoventral axis formation of the short-germ beetle Tribolium castaneum. Dev. Cell 14, 605-615.
41. 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.
42. Patel, N. H., Kornberg, T. B. and Goodman, C. S. (1989). Expression of engrailed during segmentation in grasshopper and crayfish. Development 107, 201-212.
43. Patel, N. H., Condron, B. G. and Zinn, K. (1994). Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles. Nature 367, 429-434.
44. Prpic, N. M. and Damen, W. G. (2005). Cell death during germ band inversion, dorsal closure, and nervous system development in the spider Cupiennius salei. Dev. Dyn. 234, 222-228.
45. Prpic, N. M., Wigand, B., Damen, W. G. and Klingler, M. (2001). Expression of dachshund in wild-type and Distal-less mutant Tribolium corroborates serial homologies in insect appendages. Dev. Genes Evol. 211, 467-477.
46. 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.
47. Richards, S., Gibbs, R. A., Weinstock, G. M., Brown, S. J., Denell, R., Beeman, R. W., Gibbs, R., Bucher, G., Friedrich, M., Grimmelikhuijzen, C. J. et al. (2008). The genome of the model beetle and pest Tribolium castaneum. Nature 452, 949-955.
48. Rivera-Pomar, R., Lu, X., Perrimon, N., Taubert, H. and Jackle, H. (1995). Activation of posterior gap gene expression in the Drosophila blastoderm. Nature 376, 253-256.
49. Rivera-Pomar, R., Niessing, D., Schmidt-Ott, U., Gehring, W. J. and Jackle, H. (1996). RNA binding and translational suppression by bicoid. Nature 379, 746-749.
50. Rothe, M., Wimmer, E. A., Pankratz, M. J., Gonzalez-Gaitan, M. and Jackle, H. (1994). Identical transacting factor requirement for knirps and knirps-related gene expression in the anterior but not in the posterior region of the Drosophila embryo. Mech. Dev. 46, 169-181.
51. Savard, J., Marques-Souza, H., Aranda, M. and Tautz, D. (2006). A segmentation gene in tribolium produces a polycistronic mRNA that codes for multiple conserved peptides. Cell 126, 559-569.
52. Schinko, J. B., Kreuzer, N., Offen, N., Posnien, N., Wimmer, E. A. and Bucher, G. (2008). Divergent functions of orthodenticle, empty spiracles and buttonhead in early head patterning of the beetle Tribolium castaneum (Coleoptera). Dev. Biol. 317, 600-613.
53. Schoppmeier, M. and Schroder, R. (2005). Maternal torso signaling controls body axis elongation in a short germ insect. Curr. Biol. 15, 2131-2136.
54. Schoppmeier, M., Fischer, S., Schmitt-Engel, C., Lohr, U. and Klingler, M. (2009). An ancient anterior patterning system promotes caudal repression and head formation in Ecdysozoa. Curr. Biol. 19, 1811-1815.
55. Schroder, R. (2003). The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 422, 621-625.
56. 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.
57. Small, S., Blair, A. and Levine, M. (1992). Regulation of even-skipped stripe 2 in the Drosophila embryo. EMBO J. 11, 4047-4057.
58. Sommer, R. J. and Tautz, D. (1993). Involvement of an orthologue of the Drosophila pair-rule gene hairy in segment formation of the short germ-band embryo of Tribolium (Coleoptera). Nature 361, 448-450.
59. St Johnston, D. and Nusslein-Volhard, C. (1992). The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201-219.
60. Stathopoulos, A. and Levine, M. (2002). Dorsal gradient networks in the Drosophila embryo. Dev. Biol. 246, 57-67.
61. 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. USA 96, 3786-3789.
62. 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. USA 99, 274-279.
63. Tahayato, A., Sonneville, R., Pichaud, F., Wernet, M. F., Papatsenko, D., Beaufils, P., Cook, T. and Desplan, C. (2003). Otd/Crx, a dual regulator for the specification of ommatidia subtypes in the Drosophila retina. Dev. Cell 5, 391-402.
64. Tautz, D. (1988). Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres. Nature 332, 281-284.
65. 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.
66. Tomoyasu, Y., Wheeler, S. R. and Denell, R. E. (2005). Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature 433, 643-647.
67. 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.
68. van der Zee, M., Stockhammer, O., von Levetzow, C., Nunes da Fonseca, R. and Roth, S. (2006). Sog/Chordin is required for ventral-to-dorsal Dpp/BMP transport and head formation in a short germ insect. Proc. Natl. Acad. Sci. USA 103, 16307-16312.
69. White, R. A. and Lehmann, R. (1986). A gap gene, hunchback, regulates the spatial expression of Ultrabithorax. Cell 47, 311-321.
70. Wimmer, E. A., Carleton, A., Harjes, P., Turner, T. and Desplan, C. (2000). Bicoid-independent formation of thoracic segments in Drosophila. Science 287, 2476-2479.
71. Wolff, C., Sommer, R., Schroder, 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.
72. Zeitlinger, J., Zinzen, R. P., Stark, A., Kellis, M., Zhang, H., Young, R. A. and Levine, M. (2007). Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. Genes Dev. 21, 385-390.