How Drosophila change their combs: The Hox gene Sex combs reduced and sex comb variation among Sophophora species

Evolution and Development

Volumn 10, Issue 1, 2008, Pages 121-133

  Randsholt, Neel B ^a,b,c   Santamaria, Pedro ^a,b,c  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BAB2 PROTEIN, DROSOPHILA; BRIC A BRAC PROTEIN 1, DROSOPHILA; BRIC-A-BRAC PROTEIN 1, DROSOPHILA; DACHSHUND PROTEIN, DROSOPHILA; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; NUCLEAR PROTEIN; SEX COMBS REDUCED PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

FLY; GENE; GENETICS; IDENTIFICATION METHOD; MORPHOLOGY;

ANIMAL; ARTICLE; DROSOPHILA MELANOGASTER; EVOLUTION; FEMALE; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; MALE; METABOLISM; PHYSIOLOGY; SEXUAL DEVELOPMENT;

ANIMALS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EVOLUTION; FEMALE; GENE DOSAGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; NUCLEAR PROTEINS; SEX CHARACTERISTICS; TRANSCRIPTION FACTORS;

DROSOPHILA MELANOGASTER; SOPHOPHORA;

EID: 37749035692     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/j.1525-142X.2008.00219.x     Document Type: Article

References (76)

1. Abu-Shaar, M. Mann, R. A. 1998. Generation of multiple antagonistic domains along the proximodistal axis during Drosophila leg development. Development 125 : 3821 3830.
2. Azpiazu, N. Morata, G. 2002. Distinct functions of homothorax in leg development in Drosophila. Mech. Dev. 119 : 55 67.
3. Baker, B. S. Ridge, K. A. 1980. Sex and the single cell. Genetics 94 : 383 423.
4. Barmina, O., Gonzalo, M., McIntyre, L. M. Kopp, A. 2005. Sex- and segment-specific modulation of gene expression profiles in Drosophila. Dev Biol. 288 : 528 544.
5. Basler, K. Struhl, G. 1994. Compartment boundaries and the control of Drosophila limb pattern by Hedgehog protein. Nature 368 : 208 214.
6. Boube, M., Benassayag, C., Seroudet, L. Cribbs, D. L. 1997. Rasl-mediated modulation of Drosophila homeotic function in cell and segment identity. Genetics 146 : 619 629.
7. Campbell, G. Tomlinson, A. 1995. Initiation of the proximodistal axis in insect legs. Development 121 : 619 628.
8. Campbell, G. Tomlinson, A. 1998. The roles of the homeobox genes aristaless and distal-less in patterning the legs and wings of Drosophila. Development 125 : 4483 4493.
9. Carroll, S. B., Grenier, J. K. Weatherbee, S. D. 2005. From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design. second editions. Blackwell Publishing, Oxford.
10. Chu, J., Dong, P. D. S. Panganiban, G. 2002. Limb type-specific regulation of bric-a-brac contributes to morphological diversity. Development 129 : 695 704.
11. Cline, T. W. Meyer, B. J. 1996. Vive la difference: males vs females in flies vs worms. A. Rev. Genet. 30 : 637 702.
12. Cohen, S. M., Brönner, G., Kuttner, F., Jürgens, G. Jäckle, H. 1989. Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature 338 : 432 434.
13. Cohen, S. M. Jürgens, G. 1989. Proximal-distal pattern formation in Drosophila: graded requirement for distal-less gene activity during limb development. Roux's Arch. Dev. Biol. 198 : 157 169.
14. Couderc, J. L., et al. 2002. The bric a brac locus consists of two paralogous genes encoding BTB/POZ domain proteins and acts as a homeotic and morphogenetic regulator of imaginal development in Drosophila. Development 129 : 2419 2433.
15. Diaz-Benjumea, F. J., Cohen, B. Cohen, S. M. 1994. Cell interaction between compartments establishes the proximo-distal axis of drosophila legs. Nature 372 : 175 178.
16. Docquier, F. 1997. Contrôle de l'identité cellulaire par les gènes multi sex combs et dachshund chez Drosophila melanogaster. Thèse d'Université, Paris-Sud.
17. Docquier, F., Randsholt, N. B., Deutsch, J. Santamaria, P. 1999. The 35UZ transposon of Drosophila melanogaster reveals differences in maintenance of transcriptional control between embryonic and larval stages. Int. J. Dev. Biol. 43 : 275 278.
18. Galindo, M. I., Bishop, S. A., Greig, S. Couso, J. P. 2002. Leg patterning driven by proximal-distal interactions and EGFR signaling. Science 297 : 256 259.
19. Garcia-Bellido, A. 1977. Homoeotic and atavic mutations in insects. Am. Zool. 17 : 613 629.
20. Garcia-Bellido, A. Santamaria, P. 1972. Developmental analysis of the wing disc in the mutant engrailed of Drosophila melanogaster. Genetics 72 : 87 104.
21. Gindhart, J. G. Kaufman, T. C. 1995. Identification of Polycomb and trithorax group responding elements in the regulatory region of the Drosophila homeotic gene sex combs reduced. Genetics 139 : 797 814.
22. Gindhart, J. G. Jr., King, A. N. Kaufman, T. C. 1995. Characterization of the cis-regulatory region of the Drosophila homeotic gene Sex combs reduced. Genetics 139 : 781 795.
23. Glicksman, M. A. Brower, D. L. 1988. Expression of the sex combs reduced protein in Drosophila larvae. Dev. Biol. 127 : 113 118.
24. Godt, D., Couderc, J. L., Cramto, S. E. Laski, F. 1993. Pattern formation in the limbs of Drosophila: bric à brac is expressed in both a gradient and a wave-like pattern and is required for specification and proper segmentation of the tarsus. Development 119 : 799 812.
25. Gompel, N. Carroll, S. B. 2003. Genetic mechanisms and constraints governing the evolution of correlated traits in drosophilid flies. Nature 424 : 931 935.
26. Goto, S. Hayashi, S. 1999. Proximal to distal cell communication in the Drosophila leg provides a basis for an intercalary mechanism of limb patterning. Development 126 : 3407 3413.
27. Grumbling, G., Strelets, V. the FlyBase Consortium 2006. FlyBase: anatomical data, images and queries. Nucl. Acid. Res. 34 : D484 D488
28. Hannah-Alava, A. 1958. Morphology and chaetotaxy of the legs of Drosophila melanogaster. J. Morphol. 103 : 281 310.
29. Held, L. I. Jr. 1995. Axes, boundaries and coordinates: the ABCs of fly leg development. Bioessays 17 : 721 732.
30. Held, L. I., Grimson, M. J. Du, Z. 2004. Proving an old prediction: the sex comb rotates at 16 to 24 hours after pupariation. Dros. Inf. Serv. 87 : 76 77.
31. Hersh, B. M. Carroll, S. G. 2005. Direct regulation of knot gene expression by Ultrabithorax and the evolution of cis-regulatory elements in Drosophila. Development 132 : 1567 1577.
32. Jacob, F. 1977. Evolution and tinkering. Science 196 : 400 492.
33. Jeong, S., Rokas, A. Carroll, S. B. 2006. Regulation of body pigmentation by the Abdominal-B Hox protein and its gain and loss in Drosophila Evolution. Cell 125 : 1387 1399.
34. Jiang, J. Struhl, G. 1996. Complementary and mutually exclusive activities of decapentaplegic and wingless organize axial patterning during Drosophila leg development. Cell 86 : 401 409.
35. Jurnsnich, A. V. Burtis, K. C. 1993. A positive role in differentiation for the male Doublesex protein of Drosophila. Dev. Biol. 155 : 235 249.
36. Keisman, E. L. Baker, B. S. 2001. The Drosophila sex determination hierarchy modulates wingless and decapentaplegic signaling to deploy dachshund sex-specifically in the genital imaginal disc. Development 128 : 1643 1656.
37. Kida, Y., Maeda, Y., Shiraishi, T., Suzuki, T. Ogura, T. 2004. Chick Dach1 interacts with the Smad complex and Sin3a to control AER formation and limb development along the proximodistal axis. Development 131 : 4179 4187.
38. Kim, S., Zang, R., Braunstein, E. S., Joachimial, A., Gvekl, A. Hogde, A. 2002. Structure of the retinal determination protein Dachshund reveas a DNA binding motif. Structure 10 : 787 795.
39. Kirschner, M. Gerhart, J. 1998. Evolvability. Proc. Natl. Acad. Sci. USA 95 : 8420 8427.
40. Kojima, T. 2004. The mechanism of Drosophila leg development along the proximodistal axis. Dev. Growth Differ. 46 : 115 129.
41. Kopp, A., Duncan, I., Godt, D. Carroll, S. B. 2000. Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408 : 553 559.
42. Kopp, A., Graze, R. M., Xu, S., Carroll, S. B. Nuzhdin, S. V. 2003. Quantitative trait loci responsible for variation in sexually dimorphic traits in Drosophila melanogaster. Genetics 163 : 771 787.
43. Kopp, A. True, J. R. 2002. Evolution of male sexual characters in the oriental Drosophila melanogaster species group. Evol. Dev. 4 : 278 291.
44. Kwiatowski, J. Ayala, F. J. 1999. Phylogeny of Drosophila and related genera: conflict between molecular and anatomical analyses. Mol Phylogenet Evol 13 : 319 328.
45. LaJeunesse, D. Shearn, A. 1996. Ez.: a polycomb group gene or a trithorax group gene? Development 122 : 2189 2197.
46. Lecuit, T. Cohen, S. M. 1997. Proximal-distal axis formation in the Drosophila leg. Nature 388 : 139 145.
47. Lemeunier, F., David, J., Tsacas, L. Ashburner, M. 1986. The melanogaster species group. In M. Ashburner, H. L. Carson J. N. Thompson (eds). The Genetics and Biology of Drosophila. Volume 2. Academic Press, London, pp. 147 256.
48. Mardon, G., Solomon, N. M. Rubin, G. M. 1994. Dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120 : 3473 3486.
49. Martini, S. R., Roman, G., Meuser, S., Mardon, G. Davis, R. L. 2000. The retinal determination gene, dachshund, is required for mushroom body cell differentiation. Development 127 : 2663 2672.
50. Nagoshi, R. N. Baker, B. S. 1990. Regulation of sex-specific RNA splicing at the Drosophila doublesex gene: cis-acting mutations in exon sequences alter sex-specific RNA splicing patterns. Genes Dev. 4 : 89 97.
51. Nuzhdin, S. V. Reiwitch, S. G. 2000. Are the same genes responsible for intra- and interspecific variability for sex comb tooth number in Drosophila? Heredity 84 : 97 102.
52. Pattatucci, A. M. Kaufman, T. C. 1991. The homeotic gene Sex combs reduced of Drosophila melanogaster is differentially regulated in the embryonic and imaginal stages of development. Genetics 129 : 443 461.
53. Pattatucci, A. M., Otteson, D. C. Kaufman, T. C. 1991. A functional and structural analysis of the Sex combs reduced locus of Drosophila melanogaster. Genetics 129 : 423 441.
54. Raff, E. C. Raff, R. A. 2000. Dissociability, modularity, evolvability. Evol. Dev. 2 : 235 237.
55. Remsen, J. O'Gardy, P. 2002. Phylogeny of Drosophilinae Diptera: Drosophilidae., with comments on combined analysis and character support. Mol. Phylogenet. Evol. 24 : 249 264.
56. Roch, F. Akam, M. 2000. Ultrabithorax and the control of cell morphology in Drosophila halteres. Development 127 : 97 107.
57. Rogers, B. T., Peterson, M. D. Kaufman, T. C. 1997. Evolution of the insect body plan as revealed by the sex combs reduced expression pattern. Development 124 : 149 157.
58. Rozowski, M. 2002. Establishing character correspondence for sensory organ traits in flies: sensory organ development provides insight for reconstructing character evolution. Mol. Phylogenet. Evol. 24 : 400 411.
59. Santamaria, P. 1998. Genesis versus epigenesis: the odd jobs of the Polycomb group of genes. Int. J. Dev. Biol. 42 : 463 469.
60. Santamaria, P. Randsholt, N. B. 1995. Characterization of a region of the X chromosome of Drosophila including multi sex combs (mxc), a Polycomb group gene which also functions as a tumour suppressor. Mol. Gen. Genet. 246 : 282 290.
61. Santamaria, P. Randsholt, N. B. 1998. On how the memory of determination is kept and what may happen to forgetful cells. In Chatterjee et Sanchez (eds.). Genome Analysis in Eukaryotes. Narosa, New Delhi, India, pp. 215 236.
62. Shen, W. Mardon, G. 1997. Ectopic eye development in Drosophila induced by directed dachshund expression. Development 124 : 45 52.
63. Shroff, S., Joshi, M. Orenic, T. 2007. Differential Delta expression underlies the diversity of sensory organ patterns among the legs of the Drosophila adult. Mech. Dev. 124 : 43 58.
64. Simon, J. A. Tamkun, J. W. 2002. Programming off and on states in chromatin: mechanisms of polycomb and trithorax group complexes. Curr. Opin. Genet. Dev. 12 : 210 218.
65. Southworth, J. W. Kennison, J. A. 2002. Transvection and Silencing of the Scr homeotic gene of Drosophila melanogaster. Genetics 161 : 733 746.
66. Steiner, E. 1976. Establishment of compartments in the developing leg imaginal discs of Drosophila melanogaster. Roux Arch. Dev. Biol. 180 : 9 30.
67. Stern, D. L. 1998. A role of Ultrabithorax in morphological differences between Drosophila species. Nature 396 : 463 466.
68. Struhl, G. 1982. Genes controlling segmental specification in the Drosophila thorax. Proc. Natl. Acad. Sci. USA 79 : 7380 7384.
69. Sucena, E., Delon, I., Jones, I., Payre, F. Stern, D. L. 2003. Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism. Nature 424 : 935 938.
70. Tavsanli, B. C., Ostrin, E. J., Burgess, H. K., Middlebrooks, B. W., Pham, T. A. Mardon, G. 2004. Structure-function analysis of the Drosophila retinal determination protein Dachshund. Dev. Biol. 272 : 231 247.
71. Tokunaga, C. 1961. The differentiation of a secondary sex comb under the influence of the gene engrailed in Drosophila melanogaster. Genetics 46 : 157 176.
72. True, J. R. Carroll, S. B. 2002. Gene co-option in physiological and morphological evolution. Ann. Rev. Cell Dev. Biol. 18 : 53 80.
73. Waterbury, J. A., Jackson, L. L. Schedl, P. 1999. Analysis of the doublesex female protein in Drosophila melanogaster. Role in sexual differentiation and behavior and dependence on intersex. Genetics 152 : 1653 1667.
74. Wittkopp, P. J., Haerum, B. K. Clark, A. G. 2004. Evolutionary changes in cis and trans gene regulation. Nature 430 : 85 88.
75. Wu, J. Cohen, S. M. 1999. Axis formation in the Drosophila leg: subdivision into proximal and distal domains by homothorax and distal-less. Development 126 : 109 117.
76. Yang, A. S. 2001. Modularity, evolvability, and adaptive radiations: a comparison of the hemi- and holometabolous insects. Evol. Dev. 3 : 59 72.