The Drosophila JNK pathway controls the morphogenesis of the egg dorsal appendages and micropyle.
During Drosophila oogenesis, the formation of the egg respiratory appendages and the micropyle require the shaping of anterior and dorsal follicle cells. Prior to their morphogenesis, cells of the presumptive appendages are determined by integrating dorsal-ventral and anterior-posterior positional information provided by the epidermal growth factor receptor (EGFR) and Decapentaplegic (Dpp) pathways, respectively. We show here that another signaling pathway, the Drosophila Jun-N-terminal kinase (JNK) cascade, is essential for the correct morphogenesis of the dorsal appendages and the micropyle during oogenesis. Mutant follicle cell clones of members of the JNK pathway, including DJNKK/hemipterous (hep), DJNK/basket (bsk), and Djun, block dorsal appendage formation and affect the micropyle shape and size, suggesting a late requirement for the JNK pathway in anterior chorion morphogenesis. In support of this view, hep does not affect early follicle cell patterning as indicated by the normal expression of kekkon (kek) and Broad-Complex (BR-C), two of the targets of the EGFR pathway in dorsal follicle cells. Furthermore, the expression of the TGF-beta homolog dpp, which is under the control of hep in embryos, is not coupled to JNK activity during oogenesis. We show that hep controls the expression of puckered (puc) in the follicular epithelium in a cell-autonomous manner. Since puc overexpression in the egg follicular epithelium mimics JNK appendages and micropyle phenotypes, it indicates a negative role of puc in their morphogenesis. The role of the JNK pathway in the morphogenesis of follicle cells and other epithelia during development is discussed.
Suzanne
M
M
Centro de Biología Molecular Severo Ochoa, Universidad Autónoma de Madrid, 28049 Madrid, Spain.
Perrimon
N
N
Noselli
S
S
D000818:Animals; D002465:Cell Movement; D002823:Chorion / Q000502:physiology; D004330:Drosophila; D029721:Drosophila Proteins; D005260:Female; D005697:Galactosides / Q000378:metabolism; D018507:Gene Expression Regulation, Developmental; D007150:Immunohistochemistry; D007211:Indoles / Q000378:metabolism; D019476:Insect Proteins / Q000378:metabolism; D020935:MAP Kinase Signaling System; D008856:Microscopy, Fluorescence; D048055:Mitogen-Activated Protein Kinase 8; D020929:Mitogen-Activated Protein Kinase Kinases / Q000378:metabolism; D020928:Mitogen-Activated Protein Kinases / Q000378:metabolism*; D006080:Ovarian Follicle / Q000378:metabolism; D010063:Ovum / Q000502:physiology*; D010641:Phenotype; D015398:Signal Transduction; D014018:Tissue Distribution
D029721:Drosophila Proteins; D005697:Galactosides; D007211:Indoles; D019476:Insect Proteins; C064196:dpp protein, Drosophila; D048055:Mitogen-Activated Protein Kinase 8; D020928:Mitogen-Activated Protein Kinases; C117694:Hep protein, Drosophila; D020929:Mitogen-Activated Protein Kinase Kinases; C044888:5-bromo-4-chloro-3-indolyl beta-galactoside