Mutually repressive interactions between the gap genes giant and Kruppel define middle body regions of the Drosophila embryo

Development ◽  
1991 ◽  
Vol 111 (2) ◽  
pp. 611-621 ◽  
Author(s):  
R. Kraut ◽  
M. Levine
Keyword(s):  
Gene Expression ◽  
Weak Interactions ◽  
Ectopic Expression ◽  
Early Embryo ◽  
Drosophila Embryo ◽  
Regulatory Interactions ◽  
Gap Gene ◽  
Gap Genes ◽  
Body Regions ◽  
Bona Fide

The gap genes play a key role in establishing pair-rule and homeotic stripes of gene expression in the Drosophila embryo. There is mounting evidence that overlapping gradients of gap gene expression are crucial for this process. Here we present evidence that the segmentation gene giant is a bona fide gap gene that is likely to act in concert with hunchback, Kruppel and knirps to initiate stripes of gene expression. We show that Kruppel and giant are expressed in complementary, non-overlapping sets of cells in the early embryo. These complementary patterns depend on mutually repressive interactions between the two genes. Ectopic expression of giant in early embryos results in the selective repression of Kruppel, and advanced-stage embryos show cuticular defects similar to those observed in Kruppel- mutants. This result and others suggest that the strongest regulatory interactions occur among those gap genes expressed in nonadjacent domains. We propose that the precisely balanced overlapping gradients of gap gene expression depend on these strong regulatory interactions, coupled with weak interactions between neighboring genes.

scholarly journals tarsal-less is expressed as a gap gene but has no gap gene phenotype in the moth midge Clogmia albipunctata

2018 ◽  
Vol 5 (8) ◽  
pp. 180458 ◽  
Author(s):  
Eva Jiménez-Guri ◽  
Karl R. Wotton ◽  
Johannes Jaeger
Keyword(s):  
Gene Expression ◽  
Drosophila Melanogaster ◽  
Rna Interference ◽  
Gap Gene ◽  
Gap Genes ◽  
Subtle Effect ◽  
Bona Fide ◽  
Vinegar Fly ◽  
Clogmia Albipunctata ◽  
Overlapping Domains

Gap genes are involved in segment determination during early development of the vinegar fly Drosophila melanogaster and other dipteran insects (flies, midges and mosquitoes). They are expressed in overlapping domains along the antero-posterior (A–P) axis of the blastoderm embryo. While gap domains cover the entire length of the A–P axis in Drosophila, there is a region in the blastoderm of the moth midge Clogmia albipunctata , which lacks canonical gap gene expression. Is a non-canonical gap gene functioning in this area? Here, we characterize tarsal-less ( tal ) in C. albipunctata . The homologue of tal in the flour beetle Tribolium castaneum (called milles-pattes, mlpt ) is a bona fide gap gene. We find that Ca-tal is expressed in the region previously reported as lacking gap gene expression. Using RNA interference, we study the interaction of Ca-tal with gap genes. We show that Ca-tal is regulated by gap genes, but only has a very subtle effect on tailless (Ca-tll), while not affecting other gap genes at all. Moreover, cuticle phenotypes of Ca-tal depleted embryos do not show any gap phenotype. We conclude that Ca-tal is expressed and regulated like a gap gene, but does not function as a gap gene in C. albipunctata .

scholarly journals A role of polycomb group genes in the regulation of gap gene expression in Drosophila.

Genetics ◽  
1994 ◽  
Vol 136 (4) ◽  
pp. 1341-1353 ◽  
Author(s):  
F Pelegri ◽  
R Lehmann
Keyword(s):  
Gene Expression ◽  
Small Region ◽  
Early Embryo ◽  
Polycomb Group ◽  
Drosophila Embryo ◽  
Polycomb Group Genes ◽  
Gap Gene ◽  
Anteroposterior Polarity

Abstract Anteroposterior polarity of the Drosophila embryo is initiated by the localized activities of the maternal genes, bicoid and nanos, which establish a gradient of the hunchback (hb) morphogen. nanos determines the distribution of the maternal Hb protein by regulating its translation. To identify further components of this pathway we isolated suppressors of nanos. In the absence of nanos high levels of Hb protein repress the abdomen-specific genes knirps and giant. In suppressor-of-nanos mutants, knirps and giant are expressed in spite of high Hb levels. The suppressors are alleles of Enhancer of zeste (E(z)) a member of the Polycomb group (Pc-G) of genes. We show that E(z), and likely other Pc-G genes, are required for maintaining the expression domains of knirps and giant initiated by the maternal Hb protein gradient. We have identified a small region of the knirps promoter that mediates the regulation by E(z) and hb. Because Pc-G genes are thought to control gene expression by regulating chromatin, we propose that imprinting at the chromatin level underlies the determination of anteroposterior polarity in the early embryo.

scholarly journals tarsal-less is expressed as a gap gene but has no gap gene phenotype in the moth midge Clogmia albipunctata

2018 ◽  
Author(s):  
Eva Jiménez-Guri ◽  
Karl R. Wotton ◽  
Johannes Jaeger
Keyword(s):  
Gene Expression ◽  
Drosophila Melanogaster ◽  
Rna Interference ◽  
Gap Gene ◽  
Gap Genes ◽  
Subtle Effect ◽  
Bona Fide ◽  
Vinegar Fly ◽  
Clogmia Albipunctata ◽  
Overlapping Domains

AbstractGap genes are involved in segment determination during early development of the vinegar fly Drosophila melanogaster and other dipteran insects (flies, midges, and mosquitoes). They are expressed in overlapping domains along the antero-posterior (A–P) axis of the blastoderm embryo. While gap domains cover the entire length of the A–P axis in Drosophila, there is a region in the blastoderm of the moth midge Clogmia albipunctata, which lacks canonical gap gene expression. Is a non-canonical gap gene functioning in this area? Here, we characterize tarsal-less (tal) in C. albipunctata. The homolog of tal in the flour beetle Tribolium castaneum (called milles-pattes, mlpt) is a bona fide gap gene. We find that Ca-tal is expressed in the region previously reported as lacking gap gene expression. Using RNA interference, we study the interaction of Ca-tal with gap genes. We show that Ca-tal is regulated by gap genes, but only has a very subtle effect on tailless (Catll), while not affecting other gap genes at all. Moreover, cuticle phenotypes of Ca-tal depleted embryos do not show any gap phenotype. We conclude that Ca-tal is expressed and regulated like a gap gene, but does not function as a gap gene in C. albipunctata.

Segmental polarity and identity in the abdomen of Drosophila is controlled by the relative position of gap gene expression

Development ◽  
1989 ◽  
Vol 107 (Supplement) ◽  
pp. 21-29 ◽  
Author(s):  
Ruth Lehmann ◽  
Hans Georg Frohnhöfer
Keyword(s):  
Gene Expression ◽  
Relative Concentration ◽  
Posterior Pole ◽  
Drosophila Embryo ◽  
Gene Products ◽  
Gap Gene ◽  
Gap Genes ◽  
Posterior Group ◽  
Pole Plasm ◽  
Maternal Gene

The establishment of the segmental pattern in the Drosophila embryo is directed by three sets of maternal genes: the anterior, the terminal and the posterior group of genes. Embryos derived from females mutant for one of the posterior group genes lack abdominal segmentation. This phenotype can be rescued by transplantation of posterior pole plasm into the abdominal region of mutant embryos. We transplanted posterior pole plasm into the middle of embryos mutant either for the posterior, the anterior and posterior, or all three maternal systems and monitored the segmentation pattern as well as the expression of the zygotic gap gene Krüppel in control and injected embryos. We conclude that polarity and identity of the abdominal segments do not depend on the relative concentration of posterior activity but rather on the position of gap gene expression. By changing the pattern of gap gene expression, the orientation of the abdomen can be reversed. These experiments suggest that maternal gene products act in a strictly hierarchical manner. The function of the maternal gene products becomes dispensable once the position of the zygotically expressed gap genes is determined. Subsequently the gap genes will control the pattern of the pair-rule and segment polarity genes.

scholarly journals Spatial regulation of the gap gene giant during Drosophila development

Development ◽  
1991 ◽  
Vol 111 (2) ◽  
pp. 601-609 ◽  
Author(s):  
R. Kraut ◽  
M. Levine
Keyword(s):  
Gene Dosage ◽  
Early Embryo ◽  
Early Embryogenesis ◽  
Maternal Factors ◽  
Spatial Regulation ◽  
Gap Gene ◽  
Gap Genes ◽  
Regulated Expression ◽  
Bona Fide ◽  
Protein Gradients

We describe the regulated expression of the segmentation gene giant (gt) during early embryogenesis. The gt protein is expressed in two broad gradients in precellular embryos, one in anterior regions and the other in posterior regions. Double immunolocalization studies show that the gt patterns overlap with protein gradients specified by the gap genes hunchback (hb) and knirps (kni). Analysis of all known gap mutants, as well as mutations that disrupt each of the maternal organizing centers, indicate that maternal factors are responsible for initiating gt expression, while gap genes participate in the subsequent refinement of the pattern. The maternal morphogen bicoid (bcd) initiates the anterior gt pattern, while nanos (nos) plays a role in the posterior pattern. Gene dosage studies indicate that different thresholds of the bcd gradient might trigger hb and gt expression, resulting in overlapping but noncoincident patterns of expression. We also present evidence that different concentrations of hb protein are instructive in defining the limits of kni and gt expression within the presumptive abdomen. These results suggest that gt is a bona fide gap gene, which acts with hb, Kruppel and kni to initiate striped patterns of gene expression in the early embryo.

Two distinct mechanisms for differential positioning of gene expression borders involving the Drosophila gap protein giant

Development ◽  
1998 ◽  
Vol 125 (19) ◽  
pp. 3765-3774 ◽  
Author(s):  
X. Wu ◽  
R. Vakani ◽  
S. Small
Keyword(s):  
Target Genes ◽  
Early Embryo ◽  
Drosophila Embryo ◽  
Anterior Border ◽  
Gap Gene ◽  
Gap Genes ◽  
Pair Rule Gene ◽  
Differential Positioning ◽  
Pair Rule

We have combined genetic experiments and a targeted misexpression approach to examine the role of the gap gene giant (gt) in patterning anterior regions of the Drosophila embryo. Our results suggest that gt functions in the repression of three target genes, the gap genes Kruppel (Kr) and hunchback (hb), and the pair-rule gene even-skipped (eve). The anterior border of Kr, which lies 4–5 nucleus diameters posterior to nuclei that express gt mRNA, is set by a threshold repression mechanism involving very low levels of gt protein. In contrast, gt activity is required, but not sufficient for formation of the anterior border of eve stripe 2, which lies adjacent to nuclei that express gt mRNA. We propose that gt's role in forming this border is to potentiate repressive interaction(s) mediated by other factor(s) that are also localized to anterior regions of the early embryo. Finally, gt is required for repression of zygotic hb expression in more anterior regions of the embryo. The differential responses of these target genes to gt repression are critical for the correct positioning and maintenance of segmentation stripes, and normal anterior development.

Torso signalling regulates terminal patterning in Drosophila by antagonising Groucho-mediated repression

Development ◽  
1997 ◽  
Vol 124 (19) ◽  
pp. 3827-3834 ◽  
Author(s):  
Z. Paroush ◽  
S.M. Wainwright ◽  
D. Ish-Horowicz
Keyword(s):  
Gene Expression ◽  
Dna Binding ◽  
Tyrosine Kinase ◽  
Receptor Tyrosine Kinase ◽  
Drosophila Embryo ◽  
Gap Gene ◽  
Gap Genes ◽  
Developmental Contexts

Patterning of the non-segmental termini of the Drosophila embryo depends on signalling via the Torso receptor tyrosine kinase (RTK). Activation of Torso at the poles of the embryo triggers restricted expression of the zygotic gap genes tailless (tll) and huckebein (hkb). In this paper, we show that the Groucho (Gro) corepressor acts in this process to confine terminal gap gene expression to the embryonic termini. Embryos lacking maternal gro activity display ectopic tll and hkb transcription; the former leads, in turn, to lack of abdominal expression of the Kruppel and knirps gap genes. We show that torso signalling permits terminal gap gene expression by antagonising Gro-mediated repression. Thus, the corepressor Gro is employed in diverse developmental contexts and, probably, by a variety of DNA-binding repressors.

Targeting gene expression to the head: the Drosophila orthodenticle gene is a direct target of the Bicoid morphogen

Development ◽  
1998 ◽  
Vol 125 (21) ◽  
pp. 4185-4193 ◽  
Author(s):  
Q. Gao ◽  
R. Finkelstein
Keyword(s):  
Gene Expression ◽  
Target Genes ◽  
Regulatory Element ◽  
Regulatory Region ◽  
Repeated Sequence ◽  
Drosophila Embryo ◽  
Sequence Motif ◽  
Specific Expression ◽  
Gap Gene

The Bicoid (Bcd) morphogen establishes the head and thorax of the Drosophila embryo. Bcd activates the transcription of identified target genes in the thoracic segments, but its mechanism of action in the head remains poorly understood. It has been proposed that Bcd directly activates the cephalic gap genes, which are the first zygotic genes to be expressed in the head primordium. It has also been suggested that the affinity of Bcd-binding sites in the promoters of Bcd target genes determines the posterior extent of their expression (the Gene X model). However, both these hypotheses remain untested. Here, we show that a small regulatory region upstream of the cephalic gap gene orthodenticle (otd) is sufficient to recapitulate early otd expression in the head primordium. This region contains two control elements, each capable of driving otd-like expression. The first element has consensus Bcd target sites that bind Bcd in vitro and are necessary for head-specific expression. As predicted by the Gene X model, this element has a relatively low affinity for Bcd. Surprisingly, the second regulatory element has no Bcd sites. Instead, it contains a repeated sequence motif similar to a regulatory element found in the promoters of otd-related genes in vertebrates. Our study is the first demonstration that a cephalic gap gene is directly regulated by Bcd. However, it also shows that zygotic gene expression can be targeted to the head primordium without direct Bcd regulation.

scholarly journals Odd-paired controls frequency doubling in Drosophila segmentation by altering the pair-rule gene regulatory network

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Erik Clark ◽  
Michael Akam
Keyword(s):  
Gene Expression ◽  
Gene Regulatory Network ◽  
Regulatory Network ◽  
Frequency Doubling ◽  
Drosophila Embryo ◽  
Anteroposterior Patterning ◽  
Regulatory Interactions ◽  
Pair Rule Gene ◽  
Gene Regulatory ◽  
Pair Rule

The Drosophila embryo transiently exhibits a double-segment periodicity, defined by the expression of seven 'pair-rule' genes, each in a pattern of seven stripes. At gastrulation, interactions between the pair-rule genes lead to frequency doubling and the patterning of 14 parasegment boundaries. In contrast to earlier stages of Drosophila anteroposterior patterning, this transition is not well understood. By carefully analysing the spatiotemporal dynamics of pair-rule gene expression, we demonstrate that frequency-doubling is precipitated by multiple coordinated changes to the network of regulatory interactions between the pair-rule genes. We identify the broadly expressed but temporally patterned transcription factor, Odd-paired (Opa/Zic), as the cause of these changes, and show that the patterning of the even-numbered parasegment boundaries relies on Opa-dependent regulatory interactions. Our findings indicate that the pair-rule gene regulatory network has a temporally modulated topology, permitting the pair-rule genes to play stage-specific patterning roles.

Posterior stripe expression of hunchback is driven from two promoters by a common enhancer element

Development ◽  
1995 ◽  
Vol 121 (9) ◽  
pp. 3067-3077 ◽  
Author(s):  
J.S. Margolis ◽  
M.L. Borowsky ◽  
E. Steingrimsson ◽  
C.W. Shim ◽  
J.A. Lengyel ◽  
...  
Keyword(s):  
Transcription Initiation ◽  
Initiation Site ◽  
Drosophila Embryo ◽  
Upstream Region ◽  
Enhancer Element ◽  
Gap Gene ◽  
Gap Genes ◽  
Two Phases ◽  
Necessary And Sufficient

The gap gene hunchback (hb) is required for the formation and segmentation of two regions of the Drosophila embryo, a broad anterior domain and a narrow posterior domain. Accumulation of hb transcript in the posterior of the embryo occurs in two phases, an initial cap covering the terminal 15% of the embryo followed by a stripe at the anterior edge of this region. By in situ hybridization with transcript-specific probes, we show that the cap is composed only of mRNA from the distal transcription initiation site (P1), while the later posterior stripe is composed of mRNA from both the distal and proximal (P2) transcription initiation sites. Using a series of genomic rescue constructs and promoter-lacZ fusion genes, we define a 1.4 kb fragment of the hb upstream region that is both necessary and sufficient for posterior expression. Sequences within this fragment mediate regulation by the terminal gap genes tailless (tll) and a huckebein, which direct the formation of the posterior hb stripe. We show that the tll protein binds in vitro to specific sites within the 1.4 kb posterior enhancer region, providing the first direct evidence for activation of gene expression by tll. We propose a model in which the anterior border of the posterior hb stripe is determined by tll concentration in a manner analogous to the activation of anterior hb expression by bicoid.

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