Soma-dependent modulations contribute to divergence of rhomboid expression during evolution of Drosophila eggshell morphology

Development

Volumn 134, Issue 8, 2007, Pages 1529-1537

  Nakamura, Yukio ^a   Kagesawa, Tatsuo ^a   Nishikawa, Minori ^a   Hayashi, Yoshiki ^b   Kobayashi, Satoru ^b   Niimi, Teruyuki ^c   Matsuno, Kenji ^a  

^a TOKYO UNIVERSITY OF SCIENCE   (Japan)

^b OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

Author keywords

Broad complex; Cis regulatory element; Dorsal appendage; Drosophila melanogaster; Drosophila virilis; EGFR signaling; Eggshell; Evolution; Gurken; Mirror; Rhomboid; Trans reulatory landscape

Indexed keywords

PROTEIN GURKEN; RHO FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MIRROR; TRANSFORMING GROWTH FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; DNA FLANKING REGION; DROSOPHILA MELANOGASTER; DROSOPHILA VIRILIS; EGG SHELL; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC VARIABILITY; GERM CELL; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; OVARY FOLLICLE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SOMATIC CELL; SPECIES DIFFERENCE;

ANIMALS; BODY PATTERNING; DROSOPHILA; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENHANCER ELEMENTS (GENETICS); EVOLUTION; EVOLUTION, MOLECULAR; EYE PROTEINS; FEMALE; HOMEODOMAIN PROTEINS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; OOCYTES; OVARIAN FOLLICLE; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR ALPHA;

DROSOPHILA MELANOGASTER; DROSOPHILA VIRILIS;

EID: 34248584861     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.001578     Document Type: Article

References (56)

1. Averof, M. and Patel, N. H. (1997). Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388, 682-686.
2. Barkai, N. and Shilo, B. Z. (2002). Modeling pattern formation: counting to two in the Drosophila egg. Curr. Biol. 12, R493-R495.
3. Belting, H. G., Shashikant, C. S. and Ruddle, F. H. (1998). Modification of expression and cis-regulation of Hoxc8 in the evolution of diverged axial morphology. Proc. Natl. Acad. Sci. USA 95, 2355-2360.
4. Berg, C. A. (2005). The Drosophila shell game: patterning genes and morphological change. Trends Genet. 21, 346-355.
5. Blair, S. S. (2000). Notch signaling: Fringe really is a glycosyltransferase. Curr. Biol. 10, R608-R612.
6. Bruckner, K., Perez, L., Clausen, H. and Cohen, S. (2000). Glycosyltransferase activity of Fringe modulates Notch-Delta interactions. Nature 406, 411-415.
7. Carroll, S. B., Grenier, J. K. and Weatherbee, S. D. (2001). From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design. Oxford: Blackwell Science.
8. Davidson, W. J. (2001). Genomic Regulatory Systems: Development and Evolution. San Diego: Academic Press.
9. Deng, W. M. and Bownes, M. (1997). Two signalling pathways specify localised expression of the Broad-Complex in Drosophila eggshell patterning and morphogenesis. Development 124, 4639-4647.
10. Dequier, E., Souid, S., Pal, M., Maroy, P., Lepesant, J. A. and Yanicostas, C. (2001). Top-DER- and Dpp-dependent requirements for the Drosophila fos/kayak gene in follicular epithelium morphogenesis. Mech. Dev. 106, 47-60.
11. Derheimer, F. A., MacLaren, C. M., Weasner, B. P., Alvarado, D. and Duffy, J. B. (2004). Conservation of an inhibitor of the epidermal growth factor receptor, Kekkon1, in dipterans. Genetics 166, 213-224.
12. Dorman, J. B., James, K. E., Fraser, S. E., Kiehart, D. P. and Berg, C. A. (2004). Bullwinkle is required for epithelial morphogenesis during Drosophila oogenesis. Dev. Biol. 267, 320-341.
13. Gompel, N. and Carroll, S. B. (2003). Genetic mechanisms and constraints governing the evolution of correlated traits in drosophilid flies. Nature 424, 931-935.
14. Gompel, N., Prud'homme, B., Wittkopp, P. J., Kassner, V. A. and Carroll, S. B. (2005). Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433, 481-487.
15. Handler, A. M. (2002). Use of the piggyBac transposon for germ-line transformation of insects. Insect Biochem. Mol. Biol. 32, 1211-1220.
16. Hayashi, Y., Hayashi, M. and Kobayashi, S. (2004). Nanos suppresses somatic cell fate in Drosophila germ line. Proc. Natl. Acad. Sci. USA 101, 10338-10342.
17. Hinton, H. E. (1969). Respiratory systems of insect egg shells. Annu. Rev. Entomol. 14, 343-368.
18. Ip, Y. T., Park, R. E., Kosman, D., Bier, E. and Levine, M. (1992). The dorsal gradient morphogen regulates stripes of rhomboid expression in the presumptive neuroectoderm of the Drosophila embryo. Genes Dev. 6, 1728-1739.
19. James, K. E. and Berg, C. A. (2003). Temporal comparison of Broad-Complex expression during eggshell-appendage patterning and morphogenesis in two Drosophila species with different eggshell-appendage numbers. Gene Expr. Patterns 3, 629-634.
20. Jordan, K. C., Clegg, N. J., Blasi, J. A., Morimoto, A. M., Sen, J., Stein, D., McNeill, H., Deng, W. M., Tworoger, M. and Ruohola-Baker, H. (2000). The homeobox gene mirror links EGF signalling to embryonic dorso-ventral axis formation through notch activation. Nat. Genet. 24, 429-433.
21. Jordan, K. C., Hatfield, S. D., Tworoger, M., Ward, E. J., Fischer, K. A., Bowers, S. and Ruohola-Baker, H. (2005). Genome wide analysis of transcript levels after perturbation of the EGFR pathway in the Drosophila ovary. Dev. Dyn. 232, 709-724.
22. Kambysellis, M. P. and Craddock, E. M. (1997). Ecological and reproductive shifts in the diversification of the endemic Hawaiian Drosophila. In Molecular Evolution and Adaptive Radiation (ed. T. J. Givnish and K. J. Sytsma), pp. 475-509. Cambridge: Cambridge University Press.
23. Kimmerly, W., Stultz, K., Lewis, S., Lewis, K., Lustre, V., Romero, R., Benke, J., Sun, D., Shirley, G., Martin, C. et al. (1996). A P1-based physical map of the Drosophila euchromatic genome. Genome Res. 6, 414-430.
24. Kobayashi, S., Yamada, M., Asaoka, M. and Kitamura, T. (1996). Essential role of the posterior morphogen nanos for germline development in Drosophila. Nature 380, 708-711.
25. Lee, J. R., Urban, S., Garvey, C. F. and Freeman, M. (2001). Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila. Cell 107, 161-171.
26. Margolis, J. and Spradling, A. (1995). Identification and behavior of epithelial stem cells in the Drosophila ovary. Development 121, 3797-3807.
27. Moloney, D. J., Panin, V. M., Johnston, S. H., Chen, J., Shao, L., Wilson, R., Wang, Y., Stanley, P., Irvine, K. D., Haltiwanger, R. S. et al. (2000). Fringe is a glycosyltransferase that modifies Notch. Nature 406, 369-375.
28. Nakamura, Y. and Matsuno, K. (2003). Species-specific activation of EGF receptor signaling underlies evolutionary diversity in the dorsal appendage number of the genus Drosophila eggshells. Mech. Dev. 120, 897-907.
29. Neuman-Silberberg, F. S. and Schupbach, T. (1993). The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGF alpha-like protein. Cell 75, 165-174.
30. Nilson, L. A. and Schupbach, T. (1999). EGF receptor signaling in Drosophila oogenesis. Curr. Top. Dev. Biol. 44, 203-243.
31. Patterson, J. T. and Stone, W. S. (1952). Evolution in the Genus Drosophila. New York: Macmillan.
32. Peri, F. and Roth, S. (2000). Combined activities of Gurken and decapentaplegic specify dorsal chorion structures of the Drosophila egg. Development 127, 841-850.
33. Peri, F., Bokel, C. and Roth, S. (1999). Local Gurken signaling and dynamic MAPK activation during Drosophila oogenesis. Mech. Dev. 81, 75-88.
34. Perrimon, N. and Duffy, J. B. (1998). Developmental biology. Sending all the right signals. Nature 396, 18-19.
35. Powell, J. R. (1997). Progress and Prospects in Evolutionary Biology: The Drosophila Model. New York: Oxford University Press.
36. Ruohola-Baker, H., Grell, E., Chou, T. B., Baker, D., Jan, L. Y. and Jan, Y. N. (1993). Spatially localized rhomboid is required for establishment of the dorsal-ventral axis in Drosophila oogenesis. Cell 73, 953-965.
37. Sambrook, J. and Russel, D. W. (2001). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
38. Sano, H., Nakamura, A. and Kobayashi, S. (2002). Identification of a transcriptional regulatory region for germline-specific expression of vasa gene in Drosophila melanogaster. Mech. Dev. 112, 129-139.
39. Sapir, A., Schweitzer, R. and Shilo, B. Z. (1998). Sequential activation of the EGF receptor pathway during Drosophila oogenesis establishes the dorsoventral axis. Development 125, 191-200.
40. Schupbach, T. (1987). Germ line and soma cooperate during oogenesis to establish the dorsoventral pattern of egg shell and embryo in Drosophila melanogaster. Cell 49, 699-707.
41. Schweitzer, R., Shaharabany, M., Seger, R. and Shilo, B. Z. (1995). Secreted Spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination. Genes Dev. 9, 1518-1529.
42. Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman, B. K., Nereng, K. S., Jonsson, B., Schluter, D. and Kingsley, D. M. (2004). Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428, 717-723.
43. Shvartsman, S. Y., Muratov, C. B. and Lauffenburger, D. A. (2002). Modeling and computational analysis of EGF receptor-mediated cell communication in Drosophila oogenesis. Development 129, 2577-2589.
44. Simpson, P. (2002). Evolution of development in closely related species of flies and worms. Nat. Rev. Genet. 3, 907-917.
45. Simpson, P., Woehl, R. and Usui, K. (1999). The development and evolution of bristle patterns in Diptera. Development 126, 1349-1364.
46. Spradling, A. C. (1993a). Developmental genetics of oogenesis. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez-Arias), pp. 1-70. Plainview, NY: Cold Spring Harbor Laboratory Press.
47. Spradling, A. C. (1993b). P-element mediated transformation. In Drosophila, A Practical Approach (ed. D. B. Robert), pp. 175-198. Oxford: IRC Press Limited.
48. Stern, D. L. (1998). A role of Ultrabithorax in morphological differences between Drosophila species. Nature 396, 463-466.
49. Throckmorton, L. (1962). The problem of phylogeny in the genus Drosophila. In Studies in Genetics. Vol. II (ed. M. R. Wheeler), pp. 207-343. Austin: University of Texas Publication.
50. Tzolovsky, G., Deng, W. M., Schlitt, T. and Bownes, M. (1999). The function of the broad-complex during Drosophila melanogaster oogenesis. Genetics 153, 1371-1383.
51. Urban, S., Lee, J. R. and Freeman, M. (2001). Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107, 173-182.
52. Ward, E. J. and Berg, C. A. (2005). Juxtaposition between two cell types is necessary for dorsal appendage tube formation. Mech. Dev. 122, 241-255.
53. Ward, E. J., Zhou, X., Riddiford, L. M., Berg, C. A. and Ruohola-Baker, H. (2006). Border of Notch activity establishes a boundary between the two dorsal appendage tube cell types. Dev. Biol. 297, 461-470.
54. Wasserman, J. D. and Freeman, M. (1998). An autoregulatory cascade of EGF receptor signaling patterns the Drosophila egg. Cell 95, 355-364.
55. Wittkopp, P. J., Vaccaro, K. and Carroll, S. B. (2002). Evolution of yellow gene regulation and pigmentation in Drosophila. Curr. Biol. 12, 1547-1556.
56. Zhao, D., Woolner, S. and Bownes, M. (2000). The Mirror transcription factor links signalling pathways in Drosophila oogenesis. Dev. Genes Evol. 210, 449-457.