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et al., 1999; Huang et al., 1999). In a survey of stocks infected by
Wolbachia
(M. Clark and T. L.
Karr, unpublished data), an allele of the insulin-receptor substrate gene
chico
was found to be
infected by
Wolbachia
. Mutations in
chico
are normally homozygous viable; however, only one is
viable following removal of
Wolbachia
infection, suggesting that
chico
might interact directly with
the microbe. However, interactions between
Wolbachia
in this genetic background are complex and
cannot be explained by the
chico
mutation alone but must involve other loci located on the second
and third chromosomes. Mapping of these additional loci, which may be effectors of
chico
function,
could provide valuable genetic insights into this complex genetic pathway and, as in the
sxl
4
case,
underpins the potential impact of
Wolbachia
infection on phenotypic analyses of known mutations
in
D. melanogaster
.
Genetics of Growth Control in
Drosophila
Coordination of bacterial growth with that of host replication is under stringent control. The presence
of
Wolbachia
in a speciÝc subset of tissues (usually the gonads) is further evidence of integrated
functioning of host and parasite biology. This tissue tropism is most evident in gonadal tissues,
where bacterial numbers are highest, presumably because vertical transmission of infection is
transovarial.
Wolbachia
has been detected in somatic tissues in a number of taxa, most notably in
isopods, where heavy infections in multiple tissues have been described (Rousset et al., 1992;
Juchault et al., 1994; Bouchon et al., 1998; Dobson et al., 1999). However, reproductive tissues of
germline origin are the predominant target tissue of
Wolbachia
, suggesting speciÝc mechanisms
for their deployment during development. In this regard, it is interesting to note that
Wolbachia
become incorporated within pole cells soon after fertilization in
Drosophila
(OÔNeill and Karr,
1990; HadÝeld and Axton, 1999).
Infections are closely integrated with host development, and the timing and location of bacterial
proliferation are organized in a manner that fosters bacterial transmission with minimal adverse
effects on host viability. For example, direct bacterial counts using confocal microscopy revealed
that no microbe growth occurred in the fertilized egg for a substantial period of embryonic
development (Kose and Karr, 1995). Taken together, these observations predict a mechanism (or
mechanisms) governing bacterial replication such that replication is prevented in inappropriate
cellular environments and permitted in appropriate tissues at appropriate, and speciÝc, stages in
host development. However, the mechanisms by which this is achieved are unknown.
Critical questions relevant to the prevailing model for
Wolbachia
action (the modiÝcation/rescue
model) can best be formulated when the subcellular localization and behavior of
Wolbachia
during
spermatogenesis are understood (Clark et al., 2002). Spermatogenesis in adult
Drosophila
has been
described (Lindsley and Tokuyasu, 1980; Fuller, 1993). Sperm development proceeds within an
elongated coiled tube and begins in the germinal proliferation center located at the apical hub of
the testis where the gonial stem cells and cyst progenitor cells are located
(Figure 14.2)
.
A primary
gonial cell buds off from the germline stem cell and is surrounded by two somatically derived cyst
cells that bud off the nearby cyst progenitor cells. As the primary spermatogonial cell undergoes
four rounds of mitotic division before entering meiosis, it moves down the tube of the testis away
from the apical hub. Cytokinesis is not complete in either mitosis or meiosis, the result being 64
interconnected haploid cells. Both cyst cells as well as germ cells comprise one cyst. Following
the completion of meiosis, axoneme growth occurs as the cyst elongates, eventually growing the
entire length of the testis, with the sperm nuclei toward the seminal vesicle. Following elongation,
cysts undergo individualization, the stripping away of the major mitochondrial derivative, as well
as most cytoplasmic factors via the individualization complex, a network of cytoskeletal factors.
The individualization complex is seen as a bulge proceeding along in the cyst, pushing the stripped-
away material into the waste bag, a bulge in the tail end of the cyst. The nuclear end of the cyst
becomes anchored to the terminal epithelium, followed by the coiling of tightly packed sperm tails
prior to liberation into the seminal vesicle. Fully mature, fertilization-competent sperm in the
