Early Drosophila
Development
In the last chapter, we discussed the specification of early embryonic cells by their acquisition of
different cytoplasmic determinants that had been stored in the oocyte. The cell membranes
establish the region of cytoplasm incorporated into each new blastomere, and it is thought that
the morphogenetic determinants then direct differential gene expression in these blastomeres.
During Drosophila development, however, cellular membranes do not form until after the
thirteenth nuclear division. Prior to this time, all the nuclei share a common cytoplasm, and
material can diffuse throughout the embryo. In these embryos, the specification of cell types
along anterior-posterior and dorsal-ventral axes is accomplished by the interactions of
cytoplasmic materials within the single, multinucleated cell. Moreover, the initiation of the
anterior-posterior and dorsal-ventral differences is controlled by the position of the egg within
the mother's ovary. Whereas the sperm entry site may fix the axes in ascidians and nematodes,
the fly's anterior-posterior and dorsal-ventral axes are specified by interactions between the egg
and its surrounding follicle cells.
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9.1 Drosophila fertilization. Fertilization of Drosophila can only occur in the region of the
oocyte that will become the anterior of the embryo. Morover, the sperm tail appears to stay in
this region. [Link]
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Cleavage
Most insect eggs undergo superficial cleavage, wherein a large mass of centrally located yolk
confines cleavage to the cytoplasmic rim of the egg. One of the fascinating features of this
cleavage type is that cells do not form until after the nuclei have divided. Cleavage in a
Drosophila egg is shown in Figure 9.1. The zygote nucleus undergoes several mitotic divisions
within the central portion of the egg. In Drosophila, 256 nuclei are produced by a series of eight
nuclear divisions averaging 8 minutes each. The nuclei then migrate to the periphery of the egg,
where the mitoses continue, albeit at a progressively slower rate. During the ninth division cycle,
about five nuclei reach the surface of the posterior pole of the embryo. These nuclei become
enclosed by cell membranes and generate the pole cells that give rise to the gametes of the adult.
Most of the other nuclei arrive at the periphery of the embryo at cycle 10 and then undergo four
more divisions at progressively slower rates. During these stages of nuclear division, the embryo
is called a syncytial blastoderm, meaning that all the cleavage nuclei are contained within a
common cytoplasm. No cell membranes exist other than that of the egg itself.
Figure 9.1
Superficial cleavage in a Drosophila embryo. The early divisions occur centrally. The numbers
refer to the cell cycle. At the tenth cell cycle (512-nucleus stage 2 hours after fertilization), the
pole cells form in the posterior, and the nuclei and their (more...)
Although the nuclei divide within a common cytoplasm, this does not mean that the cytoplasm is
itself uniform. Karr and Alberts (1986) have shown that each nucleus within the syncytial
blastoderm is contained within its own little territory of cytoskeletal proteins. When the nuclei
reach the periphery of the egg during the tenth cleavage cycle, each nucleus becomes surrounded
by microtubules and microfilaments. The nuclei and their associated cytoplasmic islands are
called energids. Figure 9.2 shows the nuclei and their essential microfilament and microtubule
domains in prophase of the twelfth mitotic division.
Figure 9.2
Localization of the cytoskeleton around nuclei in the syncytial blastoderm of Drosophila. A
Drosophila embryo entering the mitotic prophase of its twelfth division was sectioned and
triple-stained. (A) The nuclei were localized by a dye that binds to (more...)
Following cycle 13, the oocyte plasma membrane folds inward between the nuclei, eventually
partitioning off each somatic nucleus into a single cell (Figure 9.3). This process creates the
cellular blastoderm, in which all the cells are arranged in a single-layered jacket around the
yolky core of the egg (Turner and Mahowald 1977; Foe and Alberts 1983). Like any other cell
formation, the formation of the cellular blastoderm involves a delicate interplay between
microtubules and microfilaments. The first phase of blastoderm cellularization is characterized
by the invagination of cell membranes and their underlying actin microfilament network into the
regions between the nuclei to form furrow canals. This process can be inhibited by drugs that
block microtubules. After the furrow canals have passed the level of the nuclei, the second phase
of cellularization occurs. Here, the rate of invagination increases, and the actin-membrane
complex begins to constrict at what will be the basal end of the cell (Schejter and Wieschaus
1993; Foe et al. 1993). In Drosophila, the cellular blastoderm consists of approximately 6000
cells and is formed within 4 hours of fertilization.
Figure 9.3
Formation of the cellular blastoderm in Drosophila. (A) Developmental series showing the
progressive cellularization. (B) Confocal fluorescence photomicrographs of nuclei dividing
during the cellularization of the blastoderm. While there are no cell boundaries, (more...)
The midblastula transition
After the nuclei reach the periphery, the time required to complete each of the next four divisions
becomes progressively longer. While cycles 1–10 are each 8 minutes long, cycle 13, the last
cycle in the syncytial blastoderm, takes 25 minutes to complete. Cycle 14, in which the
Drosophila embryo forms cells (i.e., after 13 divisions), is asynchronous. Some groups of cells
complete this cycle in 75 minutes, whereas other groups of cells take 175 minutes (Figure 9.4;
Foe 1989). Transcription from the nuclei (which begins around the eleventh cycle) is greatly
enhanced at this stage. This slowdown of nuclear division and the concomitant increase in RNA
transcription is often referred to as the midblastula transition (see Chapter 8). Such a transition is
also seen in the embryos of numerous vertebrate and invertebrate phyla. The control of this
mitotic slowdown (in Xenopus, sea urchin, starfish, and Drosophila embryos) appears to be
effected by the ratio of chromatin to cytoplasm (Newport and Kirschner 1982; Edgar et al.
1986a). Edgar and his colleagues compared the early development of wild-type Drosophila
embryos with that of a haploid mutant. These haploid Drosophila embryos have half the
wild-type quantity of chromatin at each cell division. Hence a haploid embryo at the eighth cell
cycle has the same amount of chromatin that a wild-type embryo has at cell cycle 7. The
investigators found that whereas wild-type embryos formed their cellular blastoderm
immediately after the thirteenth division, the haploid embryos underwent an extra, fourteenth,
division before cellularization. Moreover, the lengths of cycles 11–14 in wild-type embryos
corresponded to those of cycles 12–15 in the haploid embryos. Thus, the haploid embryos follow
a pattern similar to that of the wild-type embryos—only they lag by one cell division.
Figure 9.4
Differences in regional rates of cell division in Drosophila embryos. (A) Expression of the string
gene correlates with cell division. In this example, a late stage 14 embryo is stained with a
radioactive nucleotide sequence that specifically recognizes (more...)
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9.2 The regulation ofDrosophila cleavage. The control of the cell cycle in Drosophila is a story
of how the zygote nucleus gradually takes control from the mRNAs and proteins stored in the
oocyte cytoplasm. [Link]
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9.3 The early development of other insects. Drosophila is a highly derived species. There are
other insect species that develop in ways very different from the “standard” fruit fly.
[Link]
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Gastrulation
At the time of midblastula transition, gastrulation begins. The first movements of Drosophila
gastrulation segregate the presumptive mesoderm, endoderm, and ectoderm. The prospective
mesoderm—about 1000 cells constituting the ventral midline of the embryo—folds inward to
produce the ventral furrow (Figure 9.5). This furrow eventually pinches off from the surface to
become a ventral tube within the embryo. It then flattens to form a layer of mesodermal tissue
beneath the ventral ectoderm. The prospective endoderm invaginates as two pockets at the
anterior and posterior ends of the ventral furrow. The pole cells are internalized along with the
endoderm. At this time, the embryo bends to form the cephalic furrow.
Figure 9.5
Gastrulation in Drosophila. (A) Ventral furrow beginning to form as cells flanking the ventral
midline invaginate. (B) Closing of ventral furrow, with mesodermal cells placed internally and
surface ectoderm flanking the ventral midline. (C) Dorsal view (more...)
The ectodermal cells on the surface and the mesoderm undergo convergence and extension,
migrating toward the ventral midline to form the germ band, a collection of cells along the
ventral midline that includes all the cells that will form the trunk of the embryo. The germ band
extends posteriorly and, perhaps because of the egg case, wraps around the top (dorsal) surface
of the embryo (Figure 9.5D). Thus, at the end of germ band formation, the cells destined to form
the most posterior larval structures are located immediately behind the future head region. At this
time, the body segments begin to appear, dividing the ectoderm and mesoderm. The germ band
then retracts, placing the presumptive posterior segments into the posterior tip of the embryo
(Figure 9.5E).
While the germ band is in its extended position, several key morphogenetic processes occur:
organogenesis, segmentation, and the segregation of the imaginal discs* (Figure 9.5e). In
addition, the nervous system forms from two regions of ventral ectoderm. As described in
Chapter 6, neuroblasts differentiate from this neurogenic ectoderm within each segment (and also
from the nonsegmented region of the head ectoderm). Therefore, in insects like Drosophila, the
nervous system is located ventrally, rather than being derived from a dorsal neural tube as in
vertebrates.
The general body plan of Drosophila is the same in the embryo, the larva, and the adult, each of
which has a distinct head end and a distinct tail end, between which are repeating segmental
units (Figure 9.7). Three of these segments form the thorax, while another eight segments form
the abdomen. Each segment of the adult fly has its own identity. The first thoracic segment, for
example, has only legs; the second thoracic segment has legs and wings; and the third thoracic
segment has legs and halteres (balancers). Thoracic and abdominal segments can also be
distinguished from each other by differences in the cuticle. How does this pattern arise? During
the past decade, the combined approaches of molecular biology, genetics, and embryology have
led to a detailed model describing how a segmented pattern is generated along the
anterior-posterior axis and how each segment is differentiated from the others.
Figure 9.7
Comparison of larval and adult segmentation in Drosophila. The three thoracic segments can be
distinguished by their appendages: T1 (prothorax) has legs only; T2 (mesothorax) has wings and
legs; T3 (metathorax) has halteres and legs.
The anterior-posterior and dorsal-ventral axes of Drosophila form at right angles to one another,
and they are both determined by the position of the oocyte within the follicle cells of the ovary.
The rest of this chapter is divided into three main parts. The first part concerns how the
anterior-posterior axis is specified and how it determines the identity of each segment. The
second part concerns how the dorsal-ventral axis is specified by the interactions between the
oocyte and its surrounding follicle cells. The third part concerns how embryonic tissues are
specified to become particular organs by their placement along these two axes.
Figure 9.6
Schematic representation of gastrulation in Drosophila. (A) and (B) are surface and cut-away
views showing the fates of the tissues immediately prior to gastrulation. (C) shows the beginning
of gastrulation as the ventral mesoderm invaginates into the (more...)
