High plasticity in epithelial morphogenesis during Insect dorsal closure

Biology Open

Volumn 2, Issue 11, 2013, Pages 1108-1118

  Panfilio, Kristen A ^a   Oberhofer, Georg ^b   Roth, Siegfried ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Amnion; Dorsal closure; Epithelial morphogenesis; Evolution of development; Extraembryonic development; Insect; Serosa; Tribolium castaneum

Indexed keywords

EID: 84978473052     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20136072     Document Type: Article

References (58)

1. Anderson, D. T. (1972). The development of holometabolous insects. In Developmental Systems: Insects, Vol. 1 (ed. S. J. Counce and C. H. Waddington). London: Academic Press.
2. Bao, R., Fischer, T., Bolognesi, R., Brown, S. J. and Friedrich, M. (2012). Parallel duplication and partial subfunctionalization of β-catenin/armadillo during insect evolution. Mol. Biol. Evol. 29, 647-662.
3. Benton, M. A., Akam, M. and Pavlopoulos, A. (2013). Cell and tissue dynamics during Tribolium embryogenesis revealed by versatile fluorescence labeling approaches. Development 140, 3210-3220.
4. Blanchard, G. B., Kabla, A. J., Schultz, N. L., Butler, L. C., Sanson, B., Gorfinkiel, N., Mahadevan, L. and Adams, R. J. (2009). Tissue tectonics: morphogenetic strain rates, cell shape change and intercalation. Nat. Methods 6, 458-464.
5. Blanchard, G. B., Murugesu, S., Adams, R. J., Martinez-Arias, A. and Gorfinkiel, N. (2010). Cytoskeletal dynamics and supracellular organisation of cell shape fluctuations during dorsal closure. Development 137, 2743-2752.
6. Blunck, H. (1914). Die Entwicklung des Dytiscus marginalis L. vom Ei bis zur Imago. Zeitschrift für wissenschaftliche Zoologie 111, 76-151.
7. Brown, S. J., Shippy, T. D., Miller, S., Bolognesi, R., Beeman, R. W., Lorenzen, M. D., Bucher, G., Wimmer, E. A. and Klingler, M. (2009). The red flour beetle, Tribolium castaneum (Coleoptera): a model for studies of development and pest biology. Cold Spring Harb. Protoc. 2009, pdb.emo126.
8. Campos-Ortega, J. A. and Hartenstein, V. (1997). The Embryonic Development Of Drosophila Melanogaster. Berlin: Springer.
9. Cobben, R. H. (1968). Evolutionary Trends In Heteroptera. Part I. Eggs, Architecture Of The Shell, Gross Embryology And Eclosion. Wageningen: Centre for Agricultural Publishing and Documentation.
10. Edwards, K. A., Demsky, M., Montague, R. A., Weymouth, N. and Kiehart, D. P. (1997). GFP-moesin illuminates actin cytoskeleton dynamics in living tissue and demonstrates cell shape changes during morphogenesis in Drosophila. Dev. Biol. 191, 103-117.
11. Enslee, E. C. and Riddiford, L. M. (1981). Blastokinesis in embryos of the bug, Pyrrhocoris apterus. A light and electron microscopic study 1. Normal blastokinesis. J. Embryol. Exp. Morphol. 61, 35-49.
12. García-Solache, M., Jaeger, J. and Akam, M. (2010). A systematic analysis of the gap gene system in the moth midge Clogmia albipunctata. Dev. Biol. 344, 306-318.
13. Goltsev, Y., Fuse, N., Frasch, M., Zinzen, R. P., Lanzaro, G. and Levine, M. (2007). Evolution of the dorsal-ventral patterning network in the mosquito, Anopheles gambiae. Development 134, 2415-2424.
14. Gorfinkiel, N., Blanchard, G. B., Adams, R. J. and Martinez Arias, A. (2009). Mechanical control of global cell behaviour during dorsal closure in Drosophila. Development 136, 1889-1898.
15. Handel, K., Grünfelder, C. G., Roth, S. and Sander, K. (2000). Tribolium embryogenesis: a SEM study of cell shapes and movements from blastoderm to serosal closure. Dev. Genes Evol. 210, 167-179.
16. Hirschler, J. (1909). Die Embryonalentwicklung von Donacia crassipes L. Zeitschrift für wissenschaftliche Zoologie 92, 627-744.
17. Hutson, M. S., Tokutake, Y., Chang, M.-S., Bloor, J. W., Venakides, S., Kiehart, D. P. and Edwards, G. S. (2003). Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300, 145-149.
18. Jacinto, A., Wood, W., Woolner, S., Hiley, C., Turner, L., Wilson, C., Martinez-Arias, A. and Martin, P. (2002a). Dynamic analysis of actin cable function during Drosophila dorsal closure. Curr. Biol. 12, 1245-1250.
19. Jacinto, A., Woolner, S. and Martin, P. (2002b). Dynamic analysis of dorsal closure in Drosophila: from genetics to cell biology. Dev. Cell 3, 9-19.
20. Jacobs, C. G. C., Rezende, G. L., Lamers, G. E. M. and van der Zee, M. (2013). The extraembryonic serosa protects the insect egg against desiccation. Proc. R. Soc. B 280, 20131082.
21. Jung, E. (1966). Untersuchungen am Ei des Speisebohnenkäfers Bruchidius obtectus Say (Coleoptera). I. Mitteilung: Entwicklungsgeschichtliche Ergebnisse zur Kennzeichnung des Eitypus. Zeitschrift für Morphologie und Ökologie der Tiere 56, 444-480.
22. Kiehart, D. P., Galbraith, C. G., Edwards, K. A., Rickoll, W. L. and Montague, R. A. (2000). Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J. Cell Biol. 149, 471-490.
23. Laplante, C. and Nilson, L. A. (2011). Asymmetric distribution of Echinoid defines the epidermal leading edge during Drosophila dorsal closure. J. Cell Biol. 192, 335-348.
24. Mahr, E. (1960). Normale Entwicklung, Pseudofurchung und die Bedeutung des Furchungszentrums im Ei des Heimchens (Gryllus domesticus). Zeitschrift für Morphologie und Ökologie der Tiere 49, 263-311.
25. Meijering, E., Dzyubachyk, O. and Smal, I. (2012). Chapter 9: Methods for cell and particle tracking. In Imaging And Spectroscopic Analysis Of Living Cells. Optical And Spectroscopic Techniques (Methods In Enzymology, Vol. 504) (ed. P. M. Conn). San Diego, CA: Academic Press.
26. Mellanby, H. (1936). The later embryology of Rhodnius prolixus. Q. J. Microsc. Sci. 79, 1-42.
27. Nishimura, M., Inoue, Y. and Hayashi, S. (2007). A wave of EGFR signaling determines cell alignment and intercalation in the Drosophila tracheal placode. Development 134, 4273-4282.
28. 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.
29. Panfilio, K. A. (2008). Extraembryonic development in insects and the acrobatics of blastokinesis. Dev. Biol. 313, 471-491.
30. Panfilio, K. A. (2009). Late extraembryonic morphogenesis and its zen (RNAi)-induced failure in the milkweed bug Oncopeltus fasciatus. Dev. Biol. 333, 297-311.
31. Panfilio, K. A. and Roth, S. (2010). Epithelial reorganization events during late extraembryonic development in a hemimetabolous insect. Dev. Biol. 340, 100-115.
32. Panfilio, K. A., Liu, P. Z., Akam, M. and Kaufman, T. C. (2006). Oncopeltus fasciatus zen is essential for serosal tissue function in katatrepsis. Dev. Biol. 292, 226-243.
33. Patten, W. (1884). The development of Phryganids, with a preliminary note on the development of Blatta germanica. Q. J. Microsc. Sci. 24, 549-602.
34. Peralta, X. G., Toyama, Y., Hutson, M. S., Montague, R., Venakides, S., Kiehart, D. P. and Edwards, G. S. (2007). Upregulation of forces and morphogenic asymmetries in dorsal closure during Drosophila development. Biophys. J. 92, 2583-2596.
35. Pétavy, G. (1975). Involution des annexes embryonnaires dans l'oeuf de Locusta migratoria migratorioïdes R. et F. (Orthoptera: Acrididae): Morphologie et histologie. Int. J. Insect Morphol. Embryol. 4, 1-22.
36. Pope, K. L. and Harris, T. J. C. (2008). Control of cell flattening and junctional remodeling during squamous epithelial morphogenesis in Drosophila. Development 135, 2227-2238.
37. Posnien, N., Schinko, J. B., Kittelmann, S. and Bucher, G. (2010). Genetics, development and composition of the insect head - a beetle's view. Arthropod Struct. Dev. 39, 399-410.
38. Rafiqi, A. M., Lemke, S., 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.
39. Rafiqi, A. M., Lemke, S. and Schmidt-Ott, U. (2010). Postgastrular zen expression is required to develop distinct amniotic and serosal epithelia in the scuttle fly Megaselia. Dev. Biol. 341, 282-290.
40. Rakshpal, R. (1962). Morphogenesis and embryonic membranes of Gryllus assimilis (Fabricius) (Orthoptera: Gryllidae). Proceedings of the Royal Entomological Society of London. Series A, General Entomology 37, 1-12.
41. Reim, I. and Frasch, M. (2005). The Dorsocross T-box genes are key components of the regulatory network controlling early cardiogenesis in Drosophila. Development 132, 4911-4925.
42. Rugendorff, A., Younossi-Hartenstein, A. and Hartenstein, V. (1994). Embryonic origin and differentiation of the Drosophila heart. Roux Arch. Dev. Biol. 203, 266-280.
43. Sarrazin, A. F., Peel, A. D. and Averof, M. (2012). A segmentation clock with twosegment periodicity in insects. Science 336, 338-341.
44. Schmidt-Ott, U. (2000). The amnioserosa is an apomorphic character of cyclorrhaphan flies. Dev. Genes Evol. 210, 373-376.
45. Schmidt-Ott, U., Rafiqi, A. M. and Lemke, S. (2010). Hox3/zen and the evolution of extraembryonic epithelia in insects. In Hox Genes: Studies From The 20th To The 21st Century (ed. J. S. Deutsch). Austin, TX: Landes Bioscience.
46. Shah, M. V., Namigai, E. K. O. and Suzuki, Y. (2011). The role of canonical Wnt signaling in leg regeneration and metamorphosis in the red flour beetle Tribolium castaneum. Mech. Dev. 128, 342-358.
47. Sokolow, A., Toyama, Y., Kiehart, D. P. and Edwards, G. S. (2012). Cell ingression and apical shape oscillations during dorsal closure in Drosophila. Biophys. J. 102, 969-979.
48. Solon, J., Kaya-Copur, A., Colombelli, J. and Brunner, D. (2009). Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 137, 1331-1342.
49. St Johnston, D. and Sanson, B. (2011). Epithelial polarity and morphogenesis. Curr. Opin. Cell Biol. 23, 540-546.
50. Stanley, M. S. M. and Grundmann, A. W. (1970). The embryonic development of Tribolium confusum. Ann. Entomol. Soc. Am. 63, 1248-1256.
51. Strindberg, H. (1915). Hauptzüge der Entwicklungsgeschichte von Sialis lutaria L. (Eine embryologische Untersuchung). Zool. Anz. 46, 167-185.
52. Tada, M. and Heisenberg, C.-P. (2012). Convergent extension: using collective cell migration and cell intercalation to shape embryos. Development 139, 3897-3904.
53. Tiegs, O. W. and Murray, F. V. (1938). The embryonic development of Calandra oryzae. Q. J. Microsc. Sci. 80, 159-273.
54. Toyama, Y., Peralta, X. G., Wells, A. R., Kiehart, D. P. and Edwards, G. S. (2008). Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science 321, 1683-1686.
55. Truckenbrodt, W. (1973). Über die Entstehung der Serosa im besamten und im unbesamten Ei von Odontotermes badius Hav. (Insecta, Isoptera). Zeitschrift für Morphologie der Tiere 76, 193-208.
56. van der Zee, M., Berns, N. and Roth, S. (2005). Distinct functions of the Tribolium zerknüllt genes in serosa specification and dorsal closure. Curr. Biol. 15, 624-636.
57. Wakimoto, B. T., Turner, F. R. and Kaufman, T. C. (1984). Defects in embryogenesis in mutants associated with the antennapedia gene complex of Drosophila melanogaster. Dev. Biol. 102, 147-172.
58. Wigand, B., Bucher, G. and Klingler, M. (1998). A simple whole mount technique for looking at Tribolium embryos. Tribolium Information Bulletin 38, 281-283.