Copyright Ó 2009 by the Genetics Society of America
DOI: 10.1534/genetics.109.107367
stall Encodes an ADAMTS Metalloprotease and Interacts Genetically With
Delta in Drosophila Ovarian Follicle Formation
Emily F. Ozdowski,*,† Yvonne M. Mowery* and Claire Cronmiller*,1
*Department of Biology, University of Virginia, Charlottesville, Virginia 22904-4328 and †Institute for Genome Sciences and Policy/Department
of Biology, Duke University Medical Center, Durham, North Carolina 27710
Manuscript received July 15, 2009
Accepted for publication September 8, 2009
ABSTRACT
Ovarian follicle formation in Drosophila melanogaster requires stall (stl) gene function, both within and
outside the ovary, for follicle individualization, stalk cell intercalation, and oocyte localization. We have
identified the stl transcript as CG3622 and confirmed the presence of three alternatively spliced isoforms,
contrary to current genome annotation. Here we show that the gene is expressed in both ovarian
and brain tissues, which is consistent with previous evidence of an ovary nonautonomous function. On
the basis of amino acid sequence, stl encodes a metalloprotease similar to the ‘‘a disintegrin and
metalloprotease with thrombospondin’’ (ADAMTS) family. Although stl mutant ovaries fail to maintain
the branched structure of the fusome and periodically show improperly localized oocytes, stl mutants do
not alter oocyte determination. Within the ovary, stl is expressed in pupal basal stalks and in adult somatic
cells of the posterior germarium and the follicular poles. Genetically, stl exhibits a strong mutant
interaction with Delta (Dl), and Dl mutant ovaries show altered stl expression patterns. Additionally, a
previously described genetic interactor, daughterless, also modulates stl expression in the somatic ovary and
may do so directly in its capacity as a basic helix-loop-helix (bHLH) transcription factor. We propose a
complex model of long-range extraovarian signaling through secretion or extracellular domain shedding,
together with local intraovarian protein modification, to explain the dual sites of Stl metalloprotease
function in oogenesis.
A N emerging picture of the regulation of oogenesis
in Drosophila includes multiple, diverse molecular
and cellular mechanisms that take place in the ovary
ters are connected by elongated fusomes through actin-
rich ring canals (Lin et al. 1994; Roper and Brown
2004). Of the 16 cystocytes, 1 retains the most fusome
itself, as well as a growing number of regulatory pro- material and differentiates into the oocyte (Lin and
cesses that act from outside the ovary to coordinate the Spradling 1995): Its nucleus remains diploid in
external/internal environmental conditions with the preparation for meiosis. The remaining 15 cells of each
founding and development of the oocyte. In the ovary germline cyst become nurse cells: Each nucleus becomes
this process requires molecular communication between polyploid to produce sufficient nutrients for the oocyte.
soma and germline for proper ce