MATERNAL-ZYGOTIC GENE INTERACTIONS DURING FORMATION OF THE DORSOVENTRAL PATTERN IN DROSOPHILA EMBRYOS

1 Laboratoire de Génétique Moléculaire des Eucaryotes du CNRS, Unité 184 de Biologie Moléculaire et de Génie Génétique de l'INSERM, Faculté de Médecine, 67085 Strasbourg Cédex, France

Maternal-zygotic interactions involving the three genes dorsal (dl), twist (twi) and snail (sna) are described. The results suggest that all three are involved in the process by which the dorsoventral pattern of the Drosophila embryo is established. First, the lethal embryonic mutant phenotypes are rather similar. In homozygous twi or sna embryos invagination of the ventral presumptive mesodermal cells fails to occur, and the resulting embryos are devoid of internal organs. This is very similar to the dominant phenotype described for dl; in the case of dl, however, the effect is a maternal one dependent on the mutant genotype of the female. Second, a synergistic interaction has been found whereby dominant lethality of twi- or sna-bearing zygotes is observed in embryos derived from heterozygous dl females at high temperature. The temperature sensitivity of this interaction permitted definition of a temperature-sensitive period which is probably that of dl. This was found to extend from approximately 12 hr prior to oviposition to 2–3 hr of embryogenesis. A zygotic action for the dl gene in addition to the maternal effect was revealed by the finding that extra doses of dl+ in the zygotes can partially rescue the dominant lethality of heterozygous twi embryos derived from heterozygous dl females. Two possible interpretations of the synergism are considered: (1) twi and sna are activated in the embryos as a result of positional signals placed in the egg as a consequence of the functioning of the dl gene during oogenesis and, thus, play a role in embryonic determination. (2) The gene products of dl+ and twi + (or sna+) combine to produce a functional molecule that is involved in the specification of dorsoventral pattern in the early embryo.

Submitted on March 21, 1983
Accepted on July 26, 1983




This article has been cited by other articles:


Home page
DevelopmentHome page
M. J. Potthoff and E. N. Olson
MEF2: a central regulator of diverse developmental programs
Development, December 1, 2007; 134(23): 4131 - 4140.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
K. B. Laursen, E. Mielke, P. Iannaccone, and E.-M. Fuchtbauer
Mechanism of Transcriptional Activation by the Proto-oncogene Twist1
J. Biol. Chem., November 30, 2007; 282(48): 34623 - 34633.
[Abstract] [Full Text] [PDF]


Home page
Genes Dev.Home page
J. Zeitlinger, R. P. Zinzen, A. Stark, M. Kellis, H. Zhang, R. A. Young, and M. Levine
Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo
Genes & Dev., February 15, 2007; 21(4): 385 - 390.
[Abstract] [Full Text] [PDF]


Home page
Jpn J Clin OncolHome page
T. Toyama, Z. Zhang, H. Iwase, H. Yamashita, Y. Ando, M. Hamaguchi, M. Mizutani, N. Kondo, T. Fujita, Y. Fujii, et al.
Low Expression of the Snail Gene is a Good Prognostic Factor in Node-Negative Invasive Ductal Carcinomas
Jpn. J. Clin. Oncol., June 1, 2006; 36(6): 357 - 363.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
A. Tapanes-Castillo and M. K. Baylies
Notch signaling patterns Drosophila mesodermal segments by regulating the bHLH transcription factor twist
Development, May 15, 2004; 131(10): 2359 - 2372.
[Abstract] [Full Text] [PDF]


Home page
J. Cell Biol.Home page
E. S. Montana and J. T. Littleton
Characterization of a hypercontraction-induced myopathy in Drosophila caused by mutations in Mhc
J. Cell Biol., March 29, 2004; 164(7): 1045 - 1054.
[Abstract] [Full Text] [PDF]


Home page
Genes Dev.Home page
A. Stathopoulos, B. Tam, M. Ronshaugen, M. Frasch, and M. Levine
pyramus and thisbe: FGF genes that pattern the mesoderm of Drosophila embryos
Genes & Dev., March 15, 2004; 18(6): 687 - 699.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. A. Wrischnik, J. R. Timmer, L. A. Megna, and T. W. Cline
Recruitment of the Proneural Gene scute to the Drosophila Sex-Determination Pathway
Genetics, December 1, 2003; 165(4): 2007 - 2027.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
A. K. Corsi, T. M. Brodigan, E. M. Jorgensen, and M. Krause
Characterization of a dominant negative C. elegans Twist mutant protein with implications for human Saethre-Chotzen syndrome
Development, January 6, 2002; 129(11): 2761 - 2772.
[Abstract] [Full Text] [PDF]


Home page
Cancer Res.Home page
T. Okubo, T. K. Truong, B. Yu, T. Itoh, J. Zhao, B. Grube, D. Zhou, and S. Chen
Down-Regulation of Promoter I.3 Activity of the Human Aromatase Gene in Breast Tissue by Zinc-finger Protein, Snail (SnaH)
Cancer Res., February 1, 2001; 61(4): 1338 - 1346.
[Abstract] [Full Text]


Home page
DevelopmentHome page
B San Martin and M Bate
Hindgut visceral mesoderm requires an ectodermal template for normal development in Drosophila
Development, January 1, 2001; 128(2): 233 - 242.
[Abstract] [PDF]


Home page
Mol. Cell. Biol.Home page
K. Hemavathy, S. C. Guru, J. Harris, J. D. Chen, and Y. T. Ip
Human Slug Is a Repressor That Localizes to Sites of Active Transcription
Mol. Cell. Biol., July 15, 2000; 20(14): 5087 - 5095.
[Abstract] [Full Text]


Home page
Genes Dev.Home page
R. H. Goodman and S. Smolik
CBP/p300 in cell growth, transformation, and development
Genes & Dev., July 1, 2000; 14(13): 1553 - 1577.
[Full Text]


Home page
DevelopmentHome page
A. K. Corsi, S. A. Kostas, A. Fire, and M. Krause
Caenorhabditis elegans twist plays an essential role in non-striated muscle development
Development, May 15, 2000; 127(10): 2041 - 2051.
[Abstract] [PDF]


Home page
J. Biol. Chem.Home page
O. Narumi, S. Mori, S. Boku, Y. Tsuji, N. Hashimoto, S.-I. Nishikawa, and Y. Yokota
OUT, a Novel Basic Helix-Loop-Helix Transcription Factor with an Id-like Inhibitory Activity
J. Biol. Chem., February 4, 2000; 275(5): 3510 - 3521.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
D. M. Neubaum and M. F. Wolfner
Mated Drosophila melanogaster Females Require a Seminal Fluid Protein, Acp36DE, to Store Sperm Efficiently
Genetics, October 1, 1999; 153(2): 845 - 857.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
T Kusch and R Reuter
Functions for Drosophila brachyenteron and forkhead in mesoderm specification and cell signalling
Development, January 9, 1999; 126(18): 3991 - 4003.
[Abstract] [PDF]


Home page
DevelopmentHome page
M. Su, M Fujioka, T Goto, and R Bodmer
The Drosophila homeobox genes zfh-1 and even-skipped are required for cardiac-specific differentiation of a numb-dependent lineage decision
Development, January 6, 1999; 126(14): 3241 - 3251.
[Abstract] [PDF]


Home page
DevelopmentHome page
P Morize, A. Christiansen, M Costa, S Parks, and E Wieschaus
Hyperactivation of the folded gastrulation pathway induces specific cell shape changes
Development, January 2, 1998; 125(4): 589 - 597.
[Abstract] [PDF]


Home page
J. Biol. Chem.Home page
Y. M. Lee, T. Park, R. A. Schulz, and Y. Kim
Twist-mediated Activation of the NK-4 Homeobox Gene in the Visceral Mesoderm of Drosophila Requires Two Distinct Clusters of E-box Regulatory Elements
J. Biol. Chem., July 11, 1997; 272(28): 17531 - 17541.
[Abstract] [Full Text] [PDF]


Home page
J. Neurosci.Home page
X. Wang, E. R. Reynolds, P. Deak, and L. M. Hall
The seizure Locus Encodes the Drosophila Homolog of the HERG Potassium Channel
J. Neurosci., February 1, 1997; 17(3): 882 - 890.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
Z Yin, X. Xu, and M Frasch
Regulation of the twist target gene tinman by modular cis-regulatory elements during early mesoderm development
Development, January 12, 1997; 124(24): 4971 - 4982.
[Abstract] [PDF]


Home page
DevelopmentHome page
K Hemavathy, X Meng, and Y. Ip
Differential regulation of gastrulation and neuroectodermal gene expression by Snail in the Drosophila embryo
Development, January 10, 1997; 124(19): 3683 - 3691.
[Abstract] [PDF]


Home page
DevelopmentHome page
J Rusch and M Levine
Regulation of a dpp target gene in the Drosophila embryo
Development, January 1, 1997; 124(2): 303 - 311.
[Abstract] [PDF]


Home page
Genes Dev.Home page
S Gisselbrecht, J B Skeath, C Q Doe, and A M Michelson
heartless encodes a fibroblast growth factor receptor (DFR1/DFGF-R2) involved in the directional migration of early mesodermal cells in the Drosophila embryo.
Genes & Dev., December 1, 1996; 10(23): 3003 - 3017.
[Abstract] [PDF]


Home page
DevelopmentHome page
N Fuse, S Hirose, and S Hayashi
Determination of wing cell fate by the escargot and snail genes in Drosophila
Development, January 4, 1996; 122(4): 1059 - 1067.
[Abstract] [PDF]


Home page
Genes Dev.Home page
Z F Chen and R R Behringer
twist is required in head mesenchyme for cranial neural tube morphogenesis.
Genes & Dev., March 15, 1995; 9(6): 686 - 699.
[Abstract] [PDF]


Home page
DevelopmentHome page
A Hilfiker, H Amrein, A Dubendorfer, R Schneiter, and R Nothiger
The gene virilizer is required for female-specific splicing controlled by Sxl, the master gene for sexual development in Drosophila
Development, January 12, 1995; 121(12): 4017 - 4026.
[Abstract] [PDF]


Home page
DevelopmentHome page
O. Borkowski, N. Brown, and M Bate
Anterior-posterior subdivision and the diversification of the mesoderm in Drosophila
Development, January 12, 1995; 121(12): 4183 - 4193.
[Abstract] [PDF]


Home page
DevelopmentHome page
K Maggert, M Levine, and M Frasch
The somatic-visceral subdivision of the embryonic mesoderm is initiated by dorsal gradient thresholds in Drosophila
Development, January 7, 1995; 121(7): 2107 - 2116.
[Abstract] [PDF]


Home page
J. Cell Sci.Home page
S Burchard, A Paululat, U Hinz, and R Renkawitz-Pohl
The mutant not enough muscles (nem) reveals reduction of the Drosophila embryonic muscle pattern
J. Cell Sci., January 4, 1995; 108(4): 1443 - 1454.
[Abstract] [PDF]


Home page
DevelopmentHome page
P. Cubas, J. Modolell, and M. Ruiz-Gomez
The helix-loop-helix extramacrochaetae protein is required for proper specification of many cell types in the Drosophila embryo
Development, September 1, 1994; 120(9): 2555 - 2566.
[Abstract] [PDF]


Home page
Genes Dev.Home page
S Gray, P Szymanski, and M Levine
Short-range repression permits multiple enhancers to function autonomously within a complex promoter.
Genes & Dev., August 1, 1994; 8(15): 1829 - 1838.
[Abstract] [PDF]


Home page
Genes Dev.Home page
J Rusch and M Levine
Regulation of the dorsal morphogen by the Toll and torso signaling pathways: a receptor tyrosine kinase selectively masks transcriptional repression.
Genes & Dev., June 1, 1994; 8(11): 1247 - 1257.
[Abstract] [PDF]


Home page
DevelopmentHome page
U Tepass, L. Fessler, A Aziz, and V Hartenstein
Embryonic origin of hemocytes and their relationship to cell death in Drosophila
Development, January 7, 1994; 120(7): 1829 - 1837.
[Abstract] [PDF]


Home page
DevelopmentHome page
K. Irvine and E Wieschaus
Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes
Development, January 4, 1994; 120(4): 827 - 841.
[Abstract] [PDF]


Home page
DevelopmentHome page
M Leptin and S Roth
Autonomy and non-autonomy in Drosophila mesoderm determination and morphogenesis
Development, January 4, 1994; 120(4): 853 - 859.
[Abstract] [PDF]


Home page
DevelopmentHome page
U Tepass and V Hartenstein
Epithelium formation in the Drosophila midgut depends on the interaction of endoderm and mesoderm
Development, January 3, 1994; 120(3): 579 - 590.
[Abstract] [PDF]


Home page
Genes Dev.Home page
S Gonzalez-Crespo and M Levine
Interactions between dorsal and helix-loop-helix proteins initiate the differentiation of the embryonic mesoderm and neuroectoderm in Drosophila.
Genes & Dev., September 1, 1993; 7(9): 1703 - 1713.
[Abstract] [PDF]


Home page
Genes Dev.Home page
N Azpiazu and M Frasch
tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila.
Genes & Dev., July 1, 1993; 7(7b): 1325 - 1340.
[Abstract] [PDF]


Home page
Genes Dev.Home page
F B Gertler, K K Hill, M J Clark, and F M Hoffmann
Dosage-sensitive modifiers of Drosophila abl tyrosine kinase function: prospero, a regulator of axonal outgrowth, and disabled, a novel tyrosine kinase substrate.
Genes & Dev., March 1, 1993; 7(3): 441 - 453.
[Abstract] [PDF]


Home page
DevelopmentHome page
R Bodmer
The gene tinman is required for specification of the heart and visceral muscles in Drosophila
Development, January 7, 1993; 118(3): 719 - 729.
[Abstract] [PDF]


Home page
DevelopmentHome page
K. Wharton, R. Ray, and W. Gelbart
An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo
Development, January 2, 1993; 117(2): 807 - 822.
[Abstract] [PDF]


Home page
DevelopmentHome page
D. E. Smith, F. Franco del Amo, and T. Gridley
Isolation of Sna, a mouse gene homologous to the Drosophila genes snail and escargot: its expression pattern suggests multiple roles during postimplantation development
Development, December 1, 1992; 116(4): 1033 - 1039.
[Abstract] [PDF]


Home page
DevelopmentHome page
J. J. Brookman, A. T. Toosy, L. S. Shashidhara, and R. A. White
The 412 retrotransposon and the development of gonadal mesoderm in Drosophila
Development, December 1, 1992; 116(4): 1185 - 1192.
[Abstract] [PDF]


Home page
Genes Dev.Home page
Y T Ip, R E Park, D Kosman, E Bier, and M Levine
The dorsal gradient morphogen regulates stripes of rhomboid expression in the presumptive neuroectoderm of the Drosophila embryo.
Genes & Dev., September 1, 1992; 6(9): 1728 - 1739.
[Abstract] [PDF]


Home page
DevelopmentHome page
U Hinz, A Wolk, and R Renkawitz-Pohl
Ultrabithorax is a regulator of beta 3 tubulin expression in the Drosophila visceral mesoderm
Development, January 11, 1992; 116(3): 543 - 554.
[Abstract] [PDF]


Home page
DevelopmentHome page
S Goode, D Wright, and A. Mahowald
The neurogenic locus brainiac cooperates with the Drosophila EGF receptor to establish the ovarian follicle and to determine its dorsal-ventral polarity
Development, January 9, 1992; 116(1): 177 - 192.
[Abstract] [PDF]


Home page
ScienceHome page
D Kosman, Y. Ip, M Levine, and K Arora
Establishment of the mesoderm-neuroectoderm boundary in the Drosophila embryo
Science, October 4, 1991; 254(5028): 118 - 122.
[Abstract] [PDF]


Home page
Genes Dev.Home page
J Jiang, D Kosman, Y T Ip, and M Levine
The dorsal morphogen gradient regulates the mesoderm determinant twist in early Drosophila embryos.
Genes & Dev., October 1, 1991; 5(10): 1881 - 1891.
[Abstract] [PDF]


Home page
Genes Dev.Home page
M Leptin
twist and snail as positive and negative regulators during Drosophila mesoderm development.
Genes & Dev., September 1, 1991; 5(9): 1568 - 1576.
[Abstract] [PDF]


Home page
Genes Dev.Home page
Y Rao, H Vaessin, L Y Jan, and Y N Jan
Neuroectoderm in Drosophila embryos is dependent on the mesoderm for positioning but not for formation.
Genes & Dev., September 1, 1991; 5(9): 1577 - 1588.
[Abstract] [PDF]


Home page
Genes Dev.Home page
S M Parkhurst and D Ish-Horowicz
wimp, a dominant maternal-effect mutation, reduces transcription of a specific subset of segmentation genes in Drosophila.
Genes & Dev., March 1, 1991; 5(3): 341 - 357.
[Abstract] [PDF]


Home page
Genes Dev.Home page
P T O'Donnell, V L Collier, K Mogami, and S I Bernstein
Ultrastructural and molecular analyses of homozygous-viable Drosophila melanogaster muscle mutants indicate there is a complex pattern of myosin heavy-chain isoform distribution.
Genes & Dev., August 1, 1989; 3(8): 1233 - 1246.
[Abstract] [PDF]


Home page
Genes Dev.Home page
V F Irish and W M Gelbart
The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo.
Genes & Dev., October 1, 1987; 1(8): 868 - 879.
[Abstract] [PDF]


Home page
Genes Dev.Home page
B. Thisse, C. Stoetzel, M. El Messal, and F. Perrin-Schmitt
Genes of the Drosophila maternal dorsal group control the specific expression of the zygotic gene twist in presumptive mesodermal cells
Genes & Dev., September 1, 1987; 1(7): 709 - 715.
[Abstract] [PDF]