Activation of the knirps locus links patterning to morphogenesis of the second wing vein in Drosophila.
The adjacent knirps (kni) and knirps-related (knrl) genes encode functionally related zinc finger transcription factors that collaborate to initiate development of the second longitudinal wing vein (L2). kni and knrl are expressed in the third instar larval wing disc in a narrow stripe of cells just anterior to the broad central zone of cells expressing high levels of the related spalt genes. Here, we identify a 1.4 kb cis-acting enhancer element from the kni locus that faithfully directs gene expression in the L2 primordium. We find that three independent ri alleles have alterations mapping within the L2-enhancer element and show that two of these observed lesions eliminate the ability of the enhancer element to direct gene expression in the L2 primordium. The L2 enhancer can be subdivided into distinct activation and repression domains. The activation domain mediates the combined action of the general wing activator Scalloped and a putative locally provided factor, the activity of which is abrogated by a single nucleotide alteration in the ri(53j) mutant. We also find that misexpression of genes in L2 that are normally expressed in veins other than L2 results in abnormal L2 development. These experiments provide a mechanistic basis for understanding how kni and knrl link AP patterning to morphogenesis of the L2 vein by orchestrating the expression of a selective subset of vein-promoting genes in the L2 primordium.
Lunde
Karen
K
Section of Cell and Developmental Biology, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0349, USA.
Trimble
Jennifer L
JL
Guichard
Annabel
A
Guss
Kirsten A
KA
Nauber
Ulrich
U
Bier
Ethan
E
D000483:Alleles; D000818:Animals; D001483:Base Sequence; D019521:Body Patterning; D004268:DNA-Binding Proteins / Q000235:genetics* / Q000378:metabolism; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism; D004331:Drosophila melanogaster / Q000235:genetics / Q000254:growth & development*; D004742:Enhancer Elements, Genetic; D018507:Gene Expression Regulation, Developmental; D017344:Genes, Insect; D017403:In Situ Hybridization; D007301:Insect Hormones / Q000378:metabolism; D008969:Molecular Sequence Data; D009024:Morphogenesis; D011485:Protein Binding; D012097:Repressor Proteins / Q000235:genetics* / Q000378:metabolism; D016415:Sequence Alignment; D014157:Transcription Factors / Q000378:metabolism; D019076:Transgenes; D014921:Wings, Animal / Q000033:anatomy & histology / Q000254:growth & development*
D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; D007301:Insect Hormones; D012097:Repressor Proteins; D014157:Transcription Factors; C074089:kni protein, Drosophila; C087984:sd protein, Drosophila