|
|
|
Vol. 12, No. 10, pp. 1474-1482, May 15, 1998
Howard Hughes Medical Institute and Laboratory of Molecular
Biology, University of Wisconsin, Madison, Wisconsin 53706 USA
Arthropods and vertebrates are constructed of many serially
homologous structures whose individual patterns are regulated by
Hox genes. The Hox-regulated target genes and developmental pathways that determine the morphological differences between any
homologous structures are not known. The differentiation of the
Drosophila haltere from the wing through the action of the Ultrabithorax (Ubx) gene is a classic example of
Hox regulation of serial homology, although no Ubx-regulated
genes in the haltere have been identified previously. Here, we show
that Ubx represses the expression of the Wingless (Wg) signaling
protein and a subset of Wg- and Decapentaplegic-activated genes such as
spalt-related, vestigial, Serum Response Factor, and
achaete-scute, whose products regulate morphological features
that differ between the wing and haltere. In addition, we found that
some genes in the same developmental pathway are independently
regulated by Ubx. Our results suggest that Ubx, and Hox genes
in general, independently and selectively regulate genes that act at
many levels of regulatory hierarchies to shape the differential
development of serially homologous structures.
[Key Words: Ultrabithorax; haltere; development; Drosophila; serial homology]
This article has been cited by other articles:
![]() |
Y. Liu, K. S. Matthews, and S. E. Bondos Multiple Intrinsically Disordered Sequences Alter DNA Binding by the Homeodomain of the Drosophila Hox Protein Ultrabithorax J. Biol. Chem., July 25, 2008; 283(30): 20874 - 20887. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. J. Elgar, J. Han, and M. V. Taylor mef2 activity levels differentially affect gene expression during Drosophila muscle development PNAS, January 22, 2008; 105(3): 918 - 923. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Stark, N. Bushati, C. H. Jan, P. Kheradpour, E. Hodges, J. Brennecke, D. P. Bartel, S. M. Cohen, and M. Kellis A single Hox locus in Drosophila produces functional microRNAs from opposite DNA strands Genes & Dev., January 1, 2008; 22(1): 8 - 13. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Ito, K.-H. Ng, T.-S. Lim, H. Yu, and E. M. Meyerowitz The Homeotic Protein AGAMOUS Controls Late Stamen Development by Regulating a Jasmonate Biosynthetic Gene in Arabidopsis PLANT CELL, November 1, 2007; 19(11): 3516 - 3529. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. M. Walsh and S. B. Carroll Collaboration between Smads and a Hox protein in target gene repression Development, October 15, 2007; 134(20): 3585 - 3592. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Prud'homme, N. Gompel, and S. B. Carroll Colloquium Papers: Emerging principles of regulatory evolution PNAS, May 15, 2007; 104(suppl_1): 8605 - 8612. [Abstract] [Full Text] [PDF] |
||||
![]() |
W. M. Knosp, C. Saneyoshi, S. Shou, H. P. Bachinger, and H. S. Stadler Elucidation, Quantitative Refinement, and in Vivo Utilization of the HOXA13 DNA Binding Site J. Biol. Chem., March 2, 2007; 282(9): 6843 - 6853. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. A. Crickmore and R. S. Mann Hox control of morphogen mobility and organ development through regulation of glypican expression Development, January 15, 2007; 134(2): 327 - 334. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. F. de Navas, D. L. Garaulet, and E. Sanchez-Herrero The Ultrabithorax Hox gene of Drosophila controls haltere size by regulating the Dpp pathway Development, November 15, 2006; 133(22): 4495 - 4506. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. H. Oakley, B. Ostman, and A. C. V. Wilson Repression and loss of gene expression outpaces activation and gain in recently duplicated fly genes PNAS, August 1, 2006; 103(31): 11637 - 11641. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. A. Crickmore and R. S. Mann Hox Control of Organ Size by Regulation of Morphogen Production and Mobility Science, July 7, 2006; 313(5783): 63 - 68. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. E. Bondos, X.-X. Tan, and K. S. Matthews Physical and Genetic Interactions Link Hox Function with Diverse Transcription Factors and Cell Signaling Proteins Mol. Cell. Proteomics, May 1, 2006; 5(5): 824 - 834. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. McSteen Branching Out: The ramosa Pathway and the Evolution of Grass Inflorescence Morphology. PLANT CELL, March 1, 2006; 18(3): 518 - 522. [Full Text] [PDF] |
||||
![]() |
E. H. Davidson and D. H. Erwin Gene Regulatory Networks and the Evolution of Animal Body Plans Science, February 10, 2006; 311(5762): 796 - 800. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Ronshaugen, F. Biemar, J. Piel, M. Levine, and E. C. Lai The Drosophila microRNA iab-4 causes a dominant homeotic transformation of halteres to wings Genes & Dev., December 15, 2005; 19(24): 2947 - 2952. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. A. MacLean II, M. K. Rao, K. M.H. Doyle, J. S. Richards, and M. F. Wilkinson Regulation of the Rhox5 Homeobox Gene in Primary Granulosa Cells: Preovulatory Expression and Dependence on SP1/SP3 and GABP Biol Reprod, December 1, 2005; 73(6): 1126 - 1134. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. M. Hersh and S. B. Carroll Direct regulation of knot gene expression by Ultrabithorax and the evolution of cis-regulatory elements in Drosophila Development, April 1, 2005; 132(7): 1567 - 1577. [Abstract] [Full Text] [PDF] |
||||
![]() |
W. M. Knosp, V. Scott, H. P. Bachinger, and H. S. Stadler HOXA13 regulates the expression of bone morphogenetic proteins 2 and 7 to control distal limb morphogenesis Development, September 15, 2004; 131(18): 4581 - 4592. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. E. Bondos, D. J. Catanese Jr., X.-X. Tan, A. Bicknell, L. Li, and K. S. Matthews Hox Transcription Factor Ultrabithorax Ib Physically and Genetically Interacts with Disconnected Interacting Protein 1, a Double-stranded RNA-binding Protein J. Biol. Chem., June 18, 2004; 279(25): 26433 - 26444. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Narbonne, F. Besse, J. Brissard-Zahraoui, A.-M. Pret, and D. Busson polyhomeotic is required for somatic cell proliferation and differentiation during ovarian follicle formation in Drosophila Development, March 15, 2004; 131(6): 1389 - 1400. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. O. Gaufo, S. Wu, and M. R. Capecchi Contribution of Hox genes to the diversity of the hindbrain sensory system Development, March 15, 2004; 131(6): 1259 - 1266. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Bort, J. P. Martinez-Barbera, R. S. P. Beddington, and K. S. Zaret Hex homeobox gene-dependent tissue positioning is required for organogenesis of the ventral pancreas Development, February 15, 2004; 131(4): 797 - 806. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. O. Gaufo, K. R. Thomas, and M. R. Capecchi Hox3 genes coordinate mechanisms of genetic suppression and activation in the generation of branchial and somatic motoneurons Development, November 1, 2003; 130(21): 5191 - 5201. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. S. Toker, Y. Teng, H. B. Ferreira, S. W. Emmons, and M. Chalfie The Caenorhabditis elegans spalt-like gene sem-4 restricts touch cell fate by repressing the selector Hox gene egl-5 and the effector gene mec-3 Development, August 15, 2003; 130(16): 3831 - 3840. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Prasad, R. Bajpai, and L. S. Shashidhara Regulation of Wingless and Vestigial expression in wing and haltere discs of Drosophila Development, April 15, 2003; 130(8): 1537 - 1547. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. Brodu, P. R. Elstob, and A. P. Gould abdominal A specifies one cell type in Drosophila by regulating one principal target gene Development, March 8, 2003; 129(12): 2957 - 2963. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. A. Baena-Lopez and A. Garcia-Bellido Genetic requirements of vestigial in the regulation of Drosophila wing development Development, January 1, 2003; 130(1): 197 - 208. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Abouheif and G. A. Wray Evolution of the Gene Network Underlying Wing Polyphenism in Ants Science, July 12, 2002; 297(5579): 249 - 252. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Rozowski and M. Akam Hox gene control of segment-specific bristle patterns in Drosophila Genes & Dev., May 1, 2002; 16(9): 1150 - 1162. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. S. Stadler, K. M. Higgins, and M. R. Capecchi Loss of Eph-receptor expression correlates with loss of cell adhesion and chondrogenic capacity in Hoxa13 mutant limbs Development, November 1, 2001; 128(21): 4177 - 4188. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Marty, M. A. Vigano, C. Ribeiro, U. Nussbaumer, N. C. Grieder, and M. Affolter A HOX complex, a repressor element and a 50 bp sequence confer regional specificity to a DPP-responsive enhancer Development, July 15, 2001; 128(14): 2833 - 2845. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. R. Finnerty Cnidarians Reveal Intermediate Stages in the Evolution of Hox Clusters and Axial Complexity Integr. Comp. Biol., June 1, 2001; 41(3): 608 - 620. [Abstract] [Full Text] [PDF] |
||||
![]() |
L Sanchez, N Gorfinkiel, and I Guerrero Sex determination genes control the development of the Drosophila genital disc, modulating the response to Hedgehog, Wingless and Decapentaplegic signals Development, January 4, 2001; 128(7): 1033 - 1043. [Abstract] [PDF] |
||||
![]() |
D. O'Keefe and J. Thomas Drosophila wing development in the absence of dorsal identity Development, January 3, 2001; 128(5): 703 - 710. [Abstract] [PDF] |
||||
![]() |
K. J. Peterson and E. H. Davidson Special Feature: Regulatory evolution and the origin of the bilaterians PNAS, April 25, 2000; 97(9): 4430 - 4433. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. J. Peterson, S. Q. Irvine, R. A. Cameron, and E. H. Davidson Special Feature: Quantitative assessment of Hox complex expression in the indirect development of the polychaete annelid Chaetopterus sp. PNAS, April 25, 2000; 97(9): 4487 - 4492. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. L. Lewis, M. DeCamillis, and R. L. Bennett Special Feature: Distinct roles of the homeotic genes Ubx and abd-A in beetle embryonic abdominal appendage development PNAS, April 25, 2000; 97(9): 4504 - 4509. [Abstract] [Full Text] [PDF] |
||||
![]() |
I Ruvinsky and J. Gibson-Brown Genetic and developmental bases of serial homology in vertebrate limb evolution Development, January 12, 2000; 127(24): 5233 - 5244. [Abstract] [PDF] |
||||
![]() |
F Roch and M Akam Ultrabithorax and the control of cell morphology in Drosophila halteres Development, January 1, 2000; 127(1): 97 - 107. [Abstract] [PDF] |
||||
![]() |
C. R. Marshall, H. A. Orr, and N. H. Patel Morphological innovation and developmental genetics PNAS, August 31, 1999; 96(18): 9995 - 9996. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. R. Breen Mutant Alleles of the Drosophila trithorax Gene Produce Common and Unusual Homeotic and Other Developmental Phenotypes Genetics, May 1, 1999; 152(1): 319 - 344. [Abstract] [Full Text] |
||||
![]() |
G. Gibson, M. Wemple, and S. van Helden Potential Variance Affecting Homeotic Ultrabithorax and Antennapedia Phenotypes in Drosophila melanogaster Genetics, March 1, 1999; 151(3): 1081 - 1091. [Abstract] [Full Text] |
||||
![]() |
H. Ryoo, T Marty, F Casares, M Affolter, and R. Mann Regulation of Hox target genes by a DNA bound Homothorax/Hox/Extradenticle complex Development, January 11, 1999; 126(22): 5137 - 5148. [Abstract] [PDF] |
||||
![]() |
G Morata and E Sanchez-Herrero Patterning mechanisms in the body trunk and the appendages of Drosophila Development, January 7, 1999; 126(13): 2823 - 2828. [Abstract] [PDF] |
||||
![]() |
R Chen, G Halder, Z Zhang, and G Mardon Signaling by the TGF-beta homolog decapentaplegic functions reiteratively within the network of genes controlling retinal cell fate determination in Drosophila Development, January 2, 1999; 126(5): 935 - 943. [Abstract] [PDF] |
||||
![]() |
C. Arenas-Mena, P. Martinez, R. A. Cameron, and E. H. Davidson Expression of the Hox gene complex in the indirect development of a sea urchin PNAS, October 27, 1998; 95(22): 13062 - 13067. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Kurata, M. J. Go, S. Artavanis-Tsakonas, and W. J. Gehring Notch signaling and the determination of appendage identity PNAS, February 29, 2000; 97(5): 2117 - 2122. [Abstract] [Full Text] [PDF] |
||||