INTRODUCTION
The Drosophila tracheal system is a stereotypical network of
interconnected tubes that supplies air to all cells of the
organism. Initially, ten tracheal placodes are defined on both
sides of the embryo, each consisting of 20 cells. The placodes
undergo two rounds of division, giving rise to the final number
of tracheal cells. All subsequent events of tracheal
morphogenesis and branch migration occur in the absence of
any further cell division (reviewed by Manning and Krasnow,
1993).
The final structure of the tracheal tree is elaborate. Each
tracheal pit gives rise to five different branches: dorsal branch
(DB), dorsal trunk (DT), visceral branch (VB), lateral trunk
anterior (LTa) and lateral posterior/ganglionic branch
(LTp/GB). The number of cells allocated to each branch is
fixed and the final structure of each branch is stereotyped,
reflecting established migration routes. Within each branch,
different cell types are formed from an originally equipotent
population of tracheal cells (Samakovlis et al., 1996a). The
cells at the termini of the branches differentiate as terminal
cells that send long hollow extensions to hypoxic tissues
(Guillemin et al., 1996). Another group of specialized cells,
termed fusion cells, establishes connections between branches
from adjacent segments (Samakovlis et al., 1996b; Tanaka-
Matakatsu et al., 1996).
This elaborate tracheal structure is set up by the concerted
activity of multiple signaling pathways, uncovered in the past
decade (reviewed by Affolter and Shilo, 2000; Zelzer and
Shilo, 2000b). The initial assignment of tracheal fates within
the population of ectodermal cells is driven by the localized
expression of the Trachealess and Drifter transcription factors
(Anderson et al., 1995; Wilk et al., 1996; Llimargas and
Casanova, 1997; Zelzer and Shilo, 2000a). Persistent
expression of these genes in the trachea provides a ‘cell
context’ for other signals that impinge on the trachea.
Prior to the onset of tracheal migration, the precise number
of cells must be allocated to each future branch. Several
signaling pathways contribute to this decision, and in many
cases parallel inputs from different pathways are responsible
for the assignment of a particular branch fate (Wappner et al.,
1997; Vincent et al., 1998; Llimargas, 2000; Llimargas and
Lawrence, 2001; Chihara and Hayashi, 2000; Glazer and Shilo,
2001).
The process of migration is guided by the FGF pathway. All
tracheal cells express the FGF receptor, Breathless (Btl)
3585 Development 129, 3585-3596 (2002)
Printed in Great Britain © The Company of Biologists Limited 2002
DEV7944
The elbow (elB) gene encodes a conserved nuclear protein
with a single zinc finger. Expression of ElB is restricted to
a specific subset of tracheal cells, namely the dorsal branch
and the lateral trunks. Stalled or aberrant migration of
these branches is observed in elB mutant embryos.
Conversely, ElB misexpression in the trachea gave rise to
absence of the visceral branch and an increase in the
number of cells forming the dorsal branch. These results
imply that the restricted expression of ElB contributes to
the specification of distinct branch fates, as reflected in
their stereotypic pattern of migration. As elB loss-of-
function tracheal phenotypes are reminiscent of defects in
Dpp signaling, the relationship between ElB and the Dpp
pathway was examined. By using pMad antibodies that
detect the activation pattern of the Dpp pathway, we show
that Dpp signaling in the trachea is not impaired in elB
mutants. In addition, expression of the Dpp target gene kni
was unaltered. The opposite is true as well, because
expression of elB is independent of Dpp signaling. ElB thus
defines a parallel input, which determines the identity of
the lateral trunk and dorsal branch cells. No ocelli (Noc) is
the Drosophila protein most similar to ElB. Mutations in
noc give rise to a similar tracheal phenotype. Noc is capable
of associating with ElB, suggesting that they can function
as a heterodimer. ElB also associates with the Groucho
protein, indicating that the complex has the capacity to
repress transcription of target genes. Indeed, in elB or noc
mutants, expanded expression of tracheal branch-specific
genes was observed.
Key words: Elbow, Noc, Zinc finger, Trachea, Branch migration,
Groucho, Drosophila
SUMMARY
Elbow and Noc define a family of zinc finger proteins controlling
morphogenesis of specific tracheal branches
Ruslan Dorfman
1
, Lillian Glazer
1
, Ulrich Weihe
2
, Mathias F. Wernet
3
and Ben-Zion Shilo
1,
*
1
Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 76100, Israel
2
EMBL, Heidelberg, Germany
3
Department of Biology, New York University, New York, USA
*Author for correspondence (e-mail: benny.shilo@weizmann.ac.il)
Accepted 13 May 2002