The internal structure of embryonic gonads
and testis development in Drosophila melanogaster
requires scrib, lgl and dlg activity in the soma
FANI PAPAGIANNOULI*
Centre for Organismal Studies (COS) Heidelberg, University of Heidelberg, Germany
ABSTRACT Interest in the mechanism leading to the formation of the germline and its differentia-
tion during Drosophila development, initiated even as soon as the first ever cloned tumour sup-
pressor gene in Drosophila, the lethal (2) giant larvae (lgl), had been identified. Further work has
shown that the lgl, as well as discs large-1 (dlg) and scribble (scrib) tumor suppressor genes code
for scaffolding proteins associated with either the cytoskeletal matrix or the septate junctions
that act in common pathways in various tissues. This study analysed the role of Dlg, Scrib and
Lgl in the embryonic gonads and testis of Drosophila melanogaster. Loss of scrib, dlg and lgl had
no effect on gonad formation, but Dlg and Scrib in the gonadal mesoderm acted critically in the
somatic wrapping of the pole cells and the internal structure of the Drosophila embryonic gonads.
Dlg also affected the incorporation of the male-specific Sox100B positive mesodermal cells into
the male embryonic gonads, yet Sox100B expression in dlg testis remained unaffected. Analysis
at later stages revealed that scrib and lgl expression in the somatic lineage of the Drosophila tes-
tis, similar to what was previously shown for dlg, was indispensable for testis development and
homeostasis, as depletion of these genes resulted in extensive testes defects. The data presented
here emphasize the somatic requirement of Scrib, Dlg and Lgl in embryonic gonads, as well as in
the Drosophila testis that underlines the importance of the somatic lineage in the establishment
and maintenance of testis formation throughout successive developmental stages.
KEY WORDS: dlg, lgl, scrib, gonads, Drosophila testis
Introduction
Great interest on polarity genes initiated after observations that
loss-of-function mutations in genes establishing and maintaining
polarity in Drosophila lead to tumor formation with invasive proper-
ties, which subsequently placed Drosophila at the center of cancer
analysis (Gateff, 1978). Application of molecular biology led to the
isolation and characterization of the frst tumor suppressor gene
(TSG), the lethal (2) giant larvae (lgl, l(2)gl or p127
lgl
) (Mechler
et al., 1985). lgl encodes a cytosolic protein which can bind to
non-muscle myosin II and to the cytoskeletal matrix along the
baso-lateral part of the epithelial plasma membrane (Strand et al.,
1994a, Strand et al., 1994b). Likewise, mutations in discs large-1
(dlg) and scribble (scrib) genes cause also tissue overgrowth phe-
notypes. Their encoded proteins associate with septate junctions
and function in the establishment and maintenance of cell polarity
(Bilder and Perrimon, 2000, Li et al., 2001, Woods et al., 1996).
Int. J. Dev. Biol. 57: 25-34 (2013)
doi: 10.1387/ijdb.120087fp
www.intjdevbiol.com
*Address correspondence to: Fani Papagiannouli. Centre for Organismal Studies (COS), Bioquant Center (BQ32, Room 403), University of Heidelberg, Im Neuen-
heimer Feld 267, D-69120 Heidelberg, Germany. Tel: +49-6221-5451-314. Fax: +49-6221-5451-485. e-mail: fani.papagiannouli@bioquant.uni-heidelberg.de
Accepted: 4 October 2012. Final, author-corrected PDF published online: 8th March 2013.
ISSN: Online 1696-3547, Print 0214-6282
© 2013 UBC Press
Printed in Spain
Abbreviations used in this paper: CySC, somatic cyst stem cell; dlg, discs large; GSC,
germline stem cell; lgl, lethal (2) giant larvae; SCC, somatic cyst cell; scrib, scribble.
Both proteins contain multiple PDZ domains that can bind to the
C-terminal tail of trans-membrane proteins, including membrane
receptors, cytoskeletal and cytosolic proteins. As polarity scaffolds
are nowadays considered to be dynamic organizing centers, that
regulate site-specifc protein targeting or exclusion from adjacent
domains and provide the guiding cues for signaling molecules
and targeted membrane insertion, studying these classical tumor
suppressors in other tissue contexts, such as the germline, has
gained new interest (Lecuit and Wieschaus, 2002, Papagiannouli
and Mechler, 2010).
During the early embryonic life of Drosophila melanogaster
the primordial germ cells, also known as pole cells, are set aside
from the somatic lineage at the posterior pole of the embryo. The
pole cells migrate through the embryo to reach the location of