Soma-to-germline interactions during Drosophila oogenesis are influenced by dose-sensitive interactions between cut and the genes cappuccino, ovariantumor and agnostic
Sm. Jackson et Ca. Berg, Soma-to-germline interactions during Drosophila oogenesis are influenced by dose-sensitive interactions between cut and the genes cappuccino, ovariantumor and agnostic, GENETICS, 153(1), 1999, pp. 289-303
The cutgene of Drosophila melanogaster encodes a homeodomain protein that r
egulates a soma-to-germline signaling pathway required for proper morpholog
y of germline cells during oogenesis. cut is required solely in somatic fol
licle cells, and when cut function is disrupted, membranes separating adjac
ent nurse cells break down and the structural integrity of the actin cytosk
eleton is compromised. To understand the mechanism by which cut expression
influences germline cell morphology, we determined whether binucleate cells
form by defective cytokinesis or by fusion of adjacent cells. Egg chambers
produced by cut, cappuccino, and chickadee mutants contained binucleate ce
lls in which ring canal remnants stained with antibodies against Hu-li tai
shao and Kelch, two proteins that are added to ring canals after cytokinesi
s is complete. In addition, defects in egg chamber morphology were observed
only in middle to late stages of oogenesis, suggesting that germline cell
cytokineses were normal in these mutants. cut exhibited dose-sensitive gene
tic interactions with cappuccino but not with chickadee or other genes that
regulate cytoskeletal function, including armadillo spaghetti squash, quai
l, spire, Src64B, and Tec29A. Genomic regions containing genes that coopera
te with cut were identified by performing a second-site noncomplementing sc
reen using a collection of chromosomal deficiencies. Sixteen regions that i
nteract with cut during oogenesis and eight regions that interact during th
e development of other tissues were identified. Genetic interactions betwee
n cut and the ovarian tumor gene were identified as a result of the screen.
In addition, the gene agnostic was found to be required during oogenesis,
and genetic interactions between cut and agnostic were revealed. These resu
lts demonstrate that a signaling path pathway regulating the morphology of
germline cells is sensitive to genetic doses of cut and the genes cappuccin
o, ovarian tumor, and agnostic. Since these genes regulate cytoskeletal fun
ction and cAMP metabolism, the cut-mediated pathway functionally links thes
e elements to preserve the cytoarchitecture of the germline cells.