Control of segmental asymmetry in Drosophila embryos.
During Drosophila development, an important aspect of body patterning is the division of the embryo into repeating morphological units referred to as parasegments. The parasegmental domains are first defined at the blastoderm stage by alternating stripes of transcripts encoded by the pair-rule genes fushi tarazu (ftz) and even-skipped (eve) and later by stripes encoded by the segment polarity genes engrailed (en) and wingless. Here, we show that the runt gene (run) is required to generate asymmetries within these parasegmental domains. Using a heat-shock-inducible run transgene, we found that ectopic run expression leads to rapid repression of eve stripes and a somewhat delayed expansion of ftz stripes. Unexpectedly, we also found that ectopic run was a rapid and potent repressor of odd-numbered en stripes. Two remarkably different segmental phenotypes were generated as a consequence of these effects. In solving the mechanisms underlying these phenotypes, we discovered that the positioning of en stripes is largely determined by the actions of negative regulators. Our data indicate that run is required to limit the domains of en expression in the odd-numbered parasegments, while the odd-skipped gene is required to limit the domains of en expression in the even-numbered parasegments. Activation of en at the anterior margins of both sets of parasegments requires the repression of run and odd by the product of the eve gene. The spatial restriction of gene expression via negative and double negative pathways such as these is likely to be a common theme during development.
Manoukian
A S
AS
Banting and Best Department of Medical Research, C.H. Best Institute, University of Toronto, Ontario, Canada.
Krause
H M
HM
D000818:Animals; D030801:Animals, Genetically Modified; D001426:Bacterial Proteins; D051792:Basic Helix-Loop-Helix Proteins; D004268:DNA-Binding Proteins / Q000235:genetics / Q000502:physiology*; D029721:Drosophila Proteins; D004331:Drosophila melanogaster / Q000196:embryology* / Q000235:genetics; D051717:Fushi Tarazu Transcription Factors; D005786:Gene Expression Regulation; D005801:Genes, Homeobox; D017344:Genes, Insect; D005813:Genes, Synthetic; D006360:Heat-Shock Proteins / Q000235:genetics; D018398:Homeodomain Proteins; D007301:Insect Hormones / Q000235:genetics / Q000502:physiology; D019476:Insect Proteins; D008954:Models, Biological; D009024:Morphogenesis; D009687:Nuclear Proteins; D010641:Phenotype; D011401:Promoter Regions, Genetic; D011518:Proto-Oncogene Proteins / Q000235:genetics / Q000502:physiology; D011993:Recombinant Fusion Proteins / Q000378:metabolism; D012097:Repressor Proteins / Q000502:physiology; D014157:Transcription Factors / Q000235:genetics / Q000502:physiology; D051155:Wnt1 Protein
D001426:Bacterial Proteins; D051792:Basic Helix-Loop-Helix Proteins; D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; D051717:Fushi Tarazu Transcription Factors; D006360:Heat-Shock Proteins; D018398:Homeodomain Proteins; D007301:Insect Hormones; D019476:Insect Proteins; D009687:Nuclear Proteins; D011518:Proto-Oncogene Proteins; D011993:Recombinant Fusion Proteins; D012097:Repressor Proteins; D014157:Transcription Factors; D051155:Wnt1 Protein; C063459:En protein, Drosophila; C052837:eve protein, Drosophila; C497169:ftz protein, Drosophila; C489235:hairy protein, Drosophila; C080833:run protein, Drosophila; C074622:wg protein, Drosophila; C061841:hairy protein, insect; C066735:odd protein, Drosophila