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Development 104 Supplement, 17-27 (1988)
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17
1988
Phenotypic comparison between maternal and zygotic genes controlling
the segmental pattern of the Drosophila embryo
RUTH LEHMANN*
MRC Laboratory of Molecular Biology, Cambridge CB22QH, UK and Max Planck Institut
filr
Entwicklungsbiologie
III, 74 Ttibingen
FRG
*Present address: Whitehead Institute, Nine Cambridge Center, Cambridge MA 02142, USA
Key words: Drosophila embryo, segmental pattern, maternal gene , zygotic gene
lntroduction
The longitudinal pattern of the Drosophila embryo is
controlled by the concerted activity of gene products
provided duritrg oogenesis (maternally active genes)
and embryogenesis (zygotically active genes). An
initially relatively coarse system of positional information laid down by maternal gene products becomes
successively refined towards the repeating pattern of
segments first by the division into domains by the
products of the zygotic gap genes and subsequently by
the action of pair-rule and segment-pol arity genes
(Ni.isslein-Volhard & Wieschaus, 1980; Ingham &
Martinez-Arias, 1986; Ingham, 1988; for review see
Akam , 1987). Maternal genes affecting anteroposterior pattern have been classified into three groups
according to their phenotype: the terminal group, the
anterior group and the posterior group (NiissleinVolhard et al. I9B7). Together the three maternal
gene groups control the establishment of the entire
segmental pattern. Embryos that lack all maternal
information show no anteroposterior pattern
(Ntisslein-Volhard et al. 1987, R.L. unpublished
data).
The information provided by the maternal genes is
interpreted by tygotic genes. The best candidates for
genes that may directly respond to the maternal
signals are the zygotic gap genes (Table 1; NtissleinVolhard & Wieschaus, 1980). The number of genes
with a 'gap' phenotype is small and each gap gene has
a distinct phenotype. Similar to mutations in
the
gap mutations cause large continuous deletions including several consecutive segments
maternal
genes
,
while the remaining structures are relatively normal.
In this article, I would like to summarize and discuss
some of the results concerning the establishment of
positional information in the egg cell and its interpretation by differential activation of. zygotic genes. The
first part deals with the properties of the posterior
group genes as they have been characterized genetically as well as by fate-map analysis. This description
should provide some idea about the methods used to
characterize phenotypic groups. In the second part,
these results will be compared to similar studies on
the anterior and terminal group. The goal of this
article is to point to the relative roles maternal
anteroposterior genes and zygotic gap genes play in
the generation of the segmented pattern.
The maternal posterior group genes and the
zygotic gen e knirps are part of the same
developmental pathway
Mutations in eight diferent genes affect the segmentation of the embryonic abdomen: knirps (NtissleinVolhard & Wieschaus, 1980; Jtirgens et al. 1984),
tudor (Boswell & Mahowald, 1985) , vasa, valois,
staufen (Schtipbach & Wieschaus, 1986), oskar,
pumilio and nanos (Lehmann & Nilsslein-Volhard,
1986 , 1987 a, unpublished data). To test whether the
products of all eight genes are involved in the same
developmental pathw?y, I studied the lethal phenotype and its origin for each locus.
(A)
The embryonic lethal phenotype
Fig. 1 shows the strongest phenotypes produced by
mutations in one of the maternal posterior group
genes , nanos, and the zygotic gene knirps (for the
wild-type pattern refer to Fig. 1). Embryos derived
from nanos females lack all abdominal segments
while the regions anterior and posterior to the
abdomen, the head-thorax region and the telson,
respectively, appear normal. However, in embryos
mutant for a strong kni allele, two abdominal segments are formed. The first abdominal segment is
1B
R. Lehmann
Table 1. Maternal and zygotic genes affecting the anteroposterior pattern
Zygotically active
Maternally active
Map
Gene
Anterior
position*
Gene
Phenotype
bicoid
84A
Deletion of head and
thorax, acron transformed to telson
exuperantia
swallow
578
5E
Weak anterior
deletions
oskar
85A
vasa
35C
tudor
57B_D
staufen
valois
55A_F
38A_E
nanos
92A
pumilio
85C
hunchback
Map
positionx
85A
Phenotype
Deletion of thorax and
gnathal region, acron
present, pA7 and A8
missing
Posterior
Terminal
torso
43E
trunk
31A-C
torsolike
fs(1) polehole
fs(I) Nasrat
l(1) polehole
93
5CD
knirps
778-F
Deletion of most of the
abdomen. A8 present
Deletion of abdomen
(excluding telson)
and pole plasm
lgiant
3,A.
Deletion of abdomen
i
Denticle band of A5-7
deleted. Also anterior
deletion]
pole plasm present
tailless
100A
Deletion of acron and
telson, excluding
stomodeum and
proctodeum
Deletion of acron
and telson
2AB
2F
Krilppel
61F
Deletion of thorax
and anterior abdomen.
Malpighian tubules
missing
* Cytological mapping.
Juxtaposition of maternal and zygotic genes of similar phenotype affecting the antero-posterior pattern. This table shows that several
maternal genes share phenotypic similarities with one zygotic gene. The gene giant has been tentatively assigned to the posterior group
because mutant embryos have defects in the abdominal region in addition to defects in the thorax and labium (Petschek et aI. 1987).
enlarged and more rows of denticles are formed than
in a wild-type abdominal segment (14-L6 instead of
6-7 in the wild type). Morphologically this segment
resembles a first abdominal segment, but by genetic
criteria (double mutant combinations with various
mutants of the Bithorax-Complex) it seems that this
segment is of mixed segmental identity (A1-A5). The
entire field acquires thoracic morphology only in kni
embryos which lack Ubx and abdA (Sanch ez-Hetrero
et al. 1985) but not in double mutants between kni and
(lbxcl (Casanova et al. 1988). The second abdominal
segment formed by a knirps embryo corresponds
morphologically as well as genetically (complete
transformation only in double-mutants with Df(3R)
P9 (Lewis , I97B)) to a normal eighth abdominal
segment.
A11 maternal posterior group genes show the strong
phenotype described for nanos. The difference in
phenotypic strength between the zygotic and maternal mutants may be due to maternally derive d kni
product. To test this idea I compared the phenotype
of homozygous kni embryos derived from a germ line
homozygous mutant for kni with those derived under
normal conditions from a heterozygous germ line.
Germ line precursor cells from the progeny of heterozygous kni flies were transplanted into sterile hosts
(for method used refer to Lehmann & NtissleinVolhard, 1"987b). The germ lines of four females were
homozygous and those of twelve were het erozygous
for kni (total number of fertile females - 34). No
difference in the mutant phenotype could be detected
between the mutant progeny. The kni gene seems
thus to be expressed exclusively by the embryo itself.
Weak alleles have been identified for kni (Ji.irgens
et al. 1954) and all seven maternal loci (Boswell &
Mahowald, 1985; Schtipbach & Wieschaus, 1986;
Lehmann & Ntisslein-Volhard, 1986, 1987a, unpublished data). It is thus possible to compare the effect
residual gene activity of any given locus has on the
final mutant pattern. The hypomorphic series of all
seven maternal genes is basically identical and has
been described earlier for the oskar allele osk3oL .
Maternal and zygotic gene control of Drosophila segmentation
With increasing phenotypic strength segments are
lost from the middle region of the abdomen (,4.4-,4'6)
while the first and the eighth abdominal segment are
most insensitive to variations in gene activity (Fi g. 2).
The phenotype of the strong, intermediate and weak
kni alleles are found as intermediates of the maternal
series (comp are Fig . 2A-D,B-E,C-F). The strong
phenotypic similarities between the maternal genes
and kni suggest a common role these genes play for
the development of the embryonic abdomen.
(B) Effect on development and fate map
Since the final lethal phenotype is the consequence of
an early developmental misrouting it is necessary to
study the origin of the pattern abnormalities observed
Fate-map changes in the
abdominal region are difficult to detect during early
development of mutant embryos because no morphological markers can be used. The anterior and
posterior dorsal folds, for example, are formed in
strong mutant embryos and the head fold is at its
normal position in all mutants with the exception of
stau where it forms more anteriorly (Schiipbach &
Wieschaus, 1986) . Shortly after the onset of gastrulation mutant embryos deviate from wild type as they
do not fully extend the germ band to the dorsal side.
in the cuticle pattern.
This effect is more pronounced in the strong maternal
mutants than in kni embryos. Later during development localized cell death occurs in the abdominal
region of all maternal mutants and kni.
At the blastoderm stage and thus prior to any
morphological deviation from wild-type development , fate map changes can be detected in mutant
embryos probed with polyclonal antibodies directed
against the product of the segmentation gene fushi
tarazu (ftz) (Carroll & Scott, 1985 , 1986; CarroII et al.
1986). In wild-type embryos at this stage , ftz protein
is expressed in seven transverse stripes separated by
stripes of non-expressing nuclei (Fig. 3A). Each
stripe is about 3-4 nuclei wide, while the seventh ftz
expressing stripe is 5-6 nuclei wide. The repeating
pattern of. ftz expression can be used to map the
segmental primordia. The primordium of the abdomen spans from the middle of the third stripe (parasegment 6, Martinez-Arias & Lawrence, 1985) to the
anterior border of the last stripe (parasegment 14)
corresponding to a region between 50 % and 20 % egg
length (0 % egg length corresponds to the posterior
pole).
For each locus , ftz expression was monitored in
embryos of different phenotypic strength (Fig . 4).
When we compare the pattern of ftz expression in
embryos that would have developed the same late
cuticle phenotype, the phenotypic series of all maternal genes is similar. A series of fate map changes
leads from the wild-type fate map with about even
spacing of
sev
en
19
ftz expressing stripes in the region
% egg length to a dramatically
changed fate map in strong mutant embryos (Fig. 38,
Carroll et al. 1986). In these only four ftz stripes can
betwe en 65 "/" and I0
be detected. The anterior border of the first stripe is
at its normal position but the first two ftz stripes and
the interstripe are expanded such that each is five to
six cells wide instead of three to four in wild type. The
third stripe is less intensely stained with the antibody
and is only found on the dorsal side. The fourth stripe
resembles from its position and size the expression
pattern of the last, seventh, wild-type stripe
(Fig. 3B). The stripes four to six are missing. The
interpretation of the strong mutant pattern is facilitated by the pattern of expression in embryos of
intermediate phenotype (Fig.3D,F,H). In the abdominal regioil, the size of the ftz expressing and nonexpressing regions becomes reduced to one to two
cells in embryos that would show single segment
deletions (Fig. 3H). In stronger mutant embryos, the
three stripes are fused into one, or less frequently
two, broad regions of expression (Fig. 3D,F) and
finally in the strongest phenotype they disappear. In
the abdominal region, we thus observe a fusion of
metameric primordia into enlarged units while in the
thoracic region (first three stripes) segmental primordia seem to expand harmoniously towards the posterior with decreasing in gene activity (Fig. 5).
A11
maternal mutants show the same fate map shifts
with the exception of mutant staufen embryos (Figs 4
and 5). stau mutations cause an expansion of the
thoracic region towards anterior and posterior. In the
most extreme mutant phenotype, the region between
the first and the third stripe (which correspond to the
primordia of the posterior maxilla, the labium and the
first, second and anterior third thoracic segments)
extends from 75 % to 40 % egg length instead of 65 %
to 48 % inwild type (Fig. 5). In the abdominal region,
segments are compressed and finally lost in a pattern
very similar to that observed in other maternal genes
(Fig . 4). Genetic and molecular results suggest that
the effect stau mutations have on the anterior fate
map reflects the role of stau in the locahzation of
bicoid product (Driever & Ntisslein-Volhard , IgBBb;
R.L. unpublished data).
The allelic series f.or knirps is rather similar to that
described for the maternal mutants (Fig . 4) but,
interestingly, changes in the fate map are restricted to
the abdominal region while the thoracic region is not
affected (Fig. 5). In extreme kni mutants, two ftz
stripes of normal position are followed by an enlarged
third stripe of normal intensity which encompasses
the circumference of the embryo and a last stripe
most likely resembling the normal seventh stripe
(Fig. 3C) (see also Ingham & Gergen, this volume).
In weak and intermediate phenotypes, segmental
20
R. Lel'trnann
Maternal and zygotic gene control of Drosophila
primordia in the abdominal region are compressed
and lost in a sequence similar to that described for the
maternal genes (compare Fig. 3C-D,E-F,G-H).
Our studies on the phenotype, fate map and
development of mutant kni embryos and embryos
derived from females mutant for each of the maternal
posterior group genes indicate a common basis for the
late mutant phenotype. In all mutants, we can detect
similar fate-map changes in the abdominal region at
the blastoderm stage (2'5h after egg deposition).
These fate-map changes presumably lead to the
generation of enlarged segmental primordia in which
cell death occurs later during development. Thus we
can visuali ze the final cuticle phenotype as the consequence of a primary defect in the blastoderm fate
map and a later-occurring size-regulative process.
(C) Maternal-zygotic interactions
The wild-type function of all maternal posterior
group genes is required for an abdomen-specific
activity localized at the posterior pole (Lehmann &
Ni.isslein-Volhard, 1986, 1987 a, unpublished data).
Transplantation of posterior pole plasm from a wildtype embryo into the abdominal region rescues the
Fig. L. The phenotype of maternal mutants and zygotic
gap mutants affecting the anteroposterior pattern.
(A) Wild type. Cuticular derivatives of the acron and the
head segments are the labrum, the cephalopharyngeal
skeleton and the sensory organs (maxilla and antenna) all
situated either inside or at the very anterior tip of the
larva. Segmentation is seen clearly in the three thoracic
and eight abdominal segments. The telson at the
posterior shows no segmental organtzatton, its most
prominent structures are the Filzkorper and spiracles that
mark the posterior opening of the trachea, the anal plate
and the anal tuft (for detailed description refer to LohsSchardin et al. 1979; Jiirgens et al. 1986; Jtirgens, L987).
(B-C) The posterior group: A11 (B, maternal phenotype)
or most (C, zygotic phenotype) abdominal segments are
deleted. (B) Embryo derived from female mutant for
nosLT . (C) Embryo homozygous mutant fot kniIIIE4s .
(D,E) The terminal group: Embryos in D (maternal
phenotype) and E (tygotic phenotype) lack the most
anterior and posterior structures, the head skeleton is
smaller and FilzkorPef, anal plate and spiracles are
missing. (D) Embryo derived from female homozygous
for torwK. (E) tlPlq embryo. (F,G) The anterior group:
thorax and head structures are missing. (F) Maternal
phenotype. Embryo derived from homozygous mutant
bcdEt female, the acron is replaced by a second telson.
(G) Zygottc phenotype. Homozygous 7r6tar embryo
derived from a homozygous hb germ line. The posterior
abdomen is duplicated anteriorly, the arrow heads point
anteroposteriorly. The star demarcates a second
phenotypic trait characteristic fot hb, the naked cuticle of
A7 and the denticle band of A8 are deleted. (H) Embryo
homozygous mutant for Ky'. cp, cephalopharyngeal
skeleto fl, t, thorax ; a, abdomen , t€ , telson ; fk, Filzkdrper.
segmentation 2l
abdominal phenotype of the maternal posterior
group mutants. For osk mutants, a quantitative
relationship between the activity found at the posterior pole and the degree to which abdominal
segmentation is affected can be established. Strong
mutant embryos contain no activity while weak alleles
have residual activity (Lehmann & Ntisslein-Volhard,
1986). The transplantation experiments further indicate that the distribution of the signal from its source,
the posterior pole to its target at the abdominal
region is graded from posterior to anterior (Lehmann
& Ni.isslein-Volhard , 1987 a). The harmonious expan-
sion of the thoracic primordia in parallel to the
enhancement of the mutant phenotype further
suggests that the requirements for the signal are
different along the anteroposterior axis. The fusion of
segmental primordia in the abdominal region, on the
other hand, does not follow a strict anterior-posterior pattern (see above) and may suggest different
requirements of the posterior signal for the activation
andf or repression of kni and neighbouring gap genes,
such as Kr and giant (Petschek et al. 1987), which
affects the development of the sixth through seventh
abdominal segment (see legend of Table L).
The differences between the phenotype of kni and
the maternal genes indicate that the maternal genes
do not exclusively act on the expression of. kni. The
effect of the maternal mutants on thorax development may well reflect the role that the maternal genes
play in controlling the expression pattern of Krtippel.
affects the development of the thorax and the
anterior abdomen (Fig. LH; Wieschaus et al. 1984)
and the Kr protein is expressed at early blastoderm in
a region between 39 % and 55 % egg length (Gaul et
al. 1987). The Kr protein domain is expanded quite
prominently towards posterior in embryos lacking the
maternal posterior gene products and only slightly
enlarged in kni (Gaul & Jlickle, 1987).
Kr
hunchback and tailless share phenotypic
similarities with the anterior and terminal group
of maternal genes
Studies on the anterior and terminal group of genes
suggest
that direct relationships similar to
those
between the posterior group genes can be established
between maternal and zygottc gap genes on the basis
of phenotypic analysis and fate mapping.
(A)
The terminal group
Five maternal genes, one gene expressed maternally
well as zygotrcally and one zygotically active gene
belong to the terminal group: torso (tor), trunk (trk)
(Schtipbach & Wieschaus, 1986) ; torsolike (tsl) (Ntisslein-Volhard et al. 1987; Frohnhofer,I9ST), fs(1)I'{asas
R. Lehmann
24
e0
rttl
70
50
30
10
o/
/o
I
Egg length
+
w
m
nanos
nanos
S
+
w
m
pumilio
bos
(')
.!m
S
U)
'aw
o+
(-)
+
w
m
oskar
c)
S
\{ /, ,rj
staufen
o<
+
w
m
vasa
S
111
+
w
m
valois
S
100
m
tudor
S
+
w
m
staufen
S
+
h
m
knirps
s
Fig. 4. Comparative fate maps of the hypomorphic series
of all posterior group genes. The ftz protein expression
patterns in mutant embryos of different allelic strength
are compared. For each genotype, the strongest (s)
phenotype is compared to wild type (+), a medium (-)
and a weak (w) phenotype. For kni the weak (*), strong
(s) and heterozygous (h) phenotype was recorded. For
each phenotype between three and five embryos were
drawn with a camera lucida and the position of ftz
expressing cells was recorded. The anterior border of the
first, the third and the seventh stripe are connected to
show the extent of shifts in the fate map. Hatched areas
indicate weak stripes, open bars indicate weak expression
on dorsal side. The anterior border of the first stripe
marks the position of the maxilla and the head fold in
wild type, the position of the third stripe overlaps with
the posterior part of the third thoracic and the anterior
part of the first abdominal segment. The anterior border
of the seventh stripe corresponds to the posterior part of
A8. Maternal genotypes; nos: nosLT f D\(3R)X43 (s),
nosRw f nosRW (m + w); pum: pumuto I pr*aso 1g'C (s),
29"C (m + w); osk: osk166 I OlSn)pxt-Io3 (s),
oslCql f oslCql (m + w); vas: vasPD I n(zr)A72 (s),
vasota f vasPD (m + w); val: valPE I offzlTW2 (s),
valRB f o1z)rw2 (m + w); tud: tudwcs f tudwcs; stau:
stauD3 f Df(2R) PC4 (s), sra r"t I ttauD3 (m + w); zygotic
genotypes: kni: 1rn{IID f kniIIID (s), knilaF f kn/aF (-),
kniF'f +
.
l'rl
90 80 70 60 50 40 30 20 10
0
Egg length (%)
+
w
knirp's
Fig. 5. Graphic interpretation of fate map changes in
nanos , staufen and knirps. The position of the anterior
border of each ftz strtpe is marked and corresponding
stripes are connected within each hypomorphic series (+,
wildtypei w, weak; m, intermediate; s, strong). The
identity of each stripe was deduced from its position and
from the pattern of deletions observed within the series.
The change in position of a given stripe along the
longitudinal axis depends on the allelic strength. The shift
in position is harmonious within the thoracic region in
nos and stau. In stau embryos, the thoracic region gets
expanded anteriorly and posteriorly. The fate map of the
thoracic region is unaffected in mutant kni embryos.
data) support the similarities in phenotype. In hb and
bcd mutant embryos, the two anterior stripes of. ftz
expression are deleted while the third stripe marking
the border between thorax and abdomen is expanded
towards anteriorly.
The extreme hb phenotype is only produced by
homozygous mutant embryos derived from a homo-
zygous mutant germ line. Such embryos form a
normal acron but almost all head structures and the
thorax and anterior abdomen are deleted. The posterior abdomen is duplicated anteriorly with the plane
of mirror-image duplication in the fourth segment
(Fig. 1G). The lack of function hb phenotype can
thus not be as easily described as a subpattern of the
more extreme maternal phenotype. Mirror-image
duplications within the abdomen occur rarely in bcd
embryos (Frohnhofer, 1987). The occurrence of mirror-image duplications in hb may be due to novel
zygotic interactions among the gap genes (Gaul &
Jiickle , 1987) caused by the lack of hb product, and
may thus point to the important role the maternal and
zygotic hb product has for controlling the expression
Maternal and zygotic gene control of Drosophila
bicoid
ANTERIOR
hunchback
Krilppel
nanos
POSTERIOR
knirps
torso
TERMINAL
tailless
ftz pattern
fate map
100
90 80 70 60 50 40 30 20 10 0 % egg length
Fig. 6. Deletion pattern of maternal and zygotic mutants
of the anterior, posterior and terminal group. Each bar
represents the pattern of deletion characteristic of either
a maternal or a zygottc mutant of the anterior, posterior
and terminal group. The hatched areas indicate deletions,
the dotted areas indicate replacements of structures, e.g.
the duplication of the telson found in bcd, or the
duplications of posterior abdominal segments in hb and
Kr. At the bottom, &tr rdealized pattern of ftz expression
is brought into register with the blastoderm fate map
(after Lohs-Schardin et al. 1979; Jiirgens et al. 1986;
Ji.irgens, L987; Campos-Ortega & Hartenstein, 1985;
Hartenstein et al. 1985). AC, acron; HE, head including
pre- as well as gnathal segmentsl T, thorax; A, abdomen;
TE, telson.
of. Kr and kni during normal development. In contrast
to the zygottc expression of hb, which is under bcd
control, the distribution of the maternal hb product is
under the influence of the maternal posterior group
genes (Tautz, 1988).
segmentation
25
and anterior group, segments are not lost in a strict
anterior-posterior order (Frohnhofer 8. NtissleinVolhard, 1987; this article), while an anterior-posterior order has been described for the terminal
group, where with increase in phenotypic strength
structures are lost towards the respective pole
(Strecker et al. 1988).
(3) Mutant phenotypes within a group originate by
similar principles (fate-map shifts, expanded segmental primordia, cell death) in the maternal and zygotic
mutants (Carroll et al. 1986; Carroll & Scott , L986;
Mlodzik et al. I9B7; Mahoney & Lengyel, 1987;
Degelmann et al. 1986; Frohnh6fer & Ntisslein-
Volhard, 1987; this article).
(4) The lack of function phenotype of each zygotic
gap gene is less extreme than that of the respective
maternal genes. Therefore, each maternal gene
seems to control the expression pattern of more than
one zygotic gene. This may be achieved by direct
activation of other zygotic genes or, as shown for
Kriippel,by suppression (Gaul & Jtickle, 1987).
A number of maternal genes and almost aII zygotic
genes have been analysed molecularly (e.g. Stephenson et al. 1987; Frigerio et al. 1986; Berlethet al. 1988;
Driever & Ni.isslein-Volhard, 1988a,b; Preiss et al.
1984; Gaul et al. 1987;Tautz et al. 1987;Tautz, 1,988).
The role of specific maternal products for the activation of the zygotic counterparts has thus become
amenable to direct molecular investigation. The
phenotypic analyses summarized here indicate a com-
plex pattern of interactions in order to provide the
information required for the establishment of an
integrated anteroposterior pattern.
I am especially thankful to Phil Ingham for his patience
and commentaries on the manuscript. I thank H. Krause for
the ftz antibody and A. Cron for help with the preparation
of the manuscript.
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