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

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.

Development ◽  
1991 ◽  
Vol 112 (3) ◽  
pp. 679-691 ◽  
Author(s):  
R. Lehmann ◽  
C. Nusslein-Volhard

A group of maternal genes, the posterior group, is required for the development of the abdominal region in the Drosophila embryo. We have used genetic as well as cytoplasmic transfer experiments to order seven of the posterior group genes (nanos, pumilio, oskar, valois, vasa, staufen and tudor) into a functional pathway. An activity present in the posterior pole plasm of wild-type embryos can restore normal abdominal development in posterior group mutants. This activity is synthesized during oogenesis and the gene nanos most likely encodes this activity. The other posterior group genes have distinct accessory functions: pumilio acts downstream of nanos and is required for the distribution or stability of the nanos-dependent activity in the embryo. Staufen, oskar, vasa, valois and tudor act upstream of nanos. Embryos from females mutant for these genes lack the specialized posterior pole plasm and consequently fail to form germ-cell precursors. We suggest that the products of these genes provide the physical structure necessary for the localization of nanos-dependent activity and of germ line determinants.


Development ◽  
1991 ◽  
Vol 111 (2) ◽  
pp. 611-621 ◽  
Author(s):  
R. Kraut ◽  
M. Levine

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.


Development ◽  
1997 ◽  
Vol 124 (19) ◽  
pp. 3827-3834 ◽  
Author(s):  
Z. Paroush ◽  
S.M. Wainwright ◽  
D. Ish-Horowicz

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.


Development ◽  
1999 ◽  
Vol 126 (4) ◽  
pp. 701-710 ◽  
Author(s):  
M.A. Pultz ◽  
J.N. Pitt ◽  
N.M. Alto

Insect axis formation is best understood in Drosophila melanogaster, where rapid anteroposterior patterning of zygotic determinants is directed by maternal gene products. The earliest zygotic control is by gap genes, which determine regions of several contiguous segments and are largely conserved in insects. We have asked genetically whether early zygotic patterning genes control similar anteroposterior domains in the parasitoid wasp Nasonia vitripennis as in Drosophila. Nasonia is advantageous for identifying and studying recessive zygotic lethal mutations because unfertilized eggs develop as males while fertilized eggs develop as females. Here we describe recessive zygotic mutations identifying three Nasonia genes: head only mutant embryos have posterior defects, resembling loss of both maternal and zygotic Drosophila caudal function; headless mutant embryos have anterior and posterior gap defects, resembling loss of both maternal and zygotic Drosophila hunchback function; squiggy mutant embryos develop only four full trunk segments, a phenotype more severe than those caused by lack of Drosophila maternal or zygotic terminal gene functions. These results indicate greater dependence on the zygotic genome to control early patterning in Nasonia than in the fly.


Development ◽  
1998 ◽  
Vol 125 (21) ◽  
pp. 4185-4193 ◽  
Author(s):  
Q. Gao ◽  
R. Finkelstein

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.


2018 ◽  
Vol 5 (8) ◽  
pp. 180458 ◽  
Author(s):  
Eva Jiménez-Guri ◽  
Karl R. Wotton ◽  
Johannes Jaeger

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 .


Development ◽  
1995 ◽  
Vol 121 (9) ◽  
pp. 3067-3077 ◽  
Author(s):  
J.S. Margolis ◽  
M.L. Borowsky ◽  
E. Steingrimsson ◽  
C.W. Shim ◽  
J.A. Lengyel ◽  
...  

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.


2021 ◽  
Author(s):  
Olivia R A Tidswell ◽  
Matthew A Benton ◽  
Michael E Akam

In Drosophila, segmentation genes of the gap class form a regulatory network that positions segment boundaries and assigns segment identities. This gene network shows striking parallels with another gene network known as the neuroblast timer series. The neuroblast timer genes hunchback, Krüppel, nubbin, and castor are expressed in temporal sequence in neural stem cells to regulate the fate of their progeny. These same four genes are expressed in corresponding spatial sequence along the Drosophila blastoderm. The first two, hunchback and Krüppel, are canonical gap genes, but nubbin and castor have limited or no roles in Drosophila segmentation. Whether nubbin and castor regulate segmentation in insects with the ancestral, sequential mode of segmentation remains largely unexplored. We have investigated the expression and functions of nubbin and castor during segment patterning in the sequentially-segmenting beetle Tribolium. Using multiplex fluorescent in situ hybridisation, we show that Tc-hunchback, Tc-Krüppel, Tc-nubbin and Tc-castor are expressed sequentially in the segment addition zone of Tribolium, in the same order as they are expressed in Drosophila neuroblasts. Furthermore, simultaneous disruption of multiple genes reveals that Tc-nubbin regulates segment identity, but does so redundantly with two previously described gap/gap-like genes, Tc-giant and Tc-knirps. Knockdown of two or more of these genes results in the formation of up to seven pairs of ectopic legs on abdominal segments. We show that this homeotic transformation is caused by loss of abdominal Hox gene expression, likely due to expanded Tc-Krüppel expression. Our findings support the theory that the neuroblast timer series was co-opted for use in insect segment patterning, and contribute to our growing understanding of the evolution and function of the gap gene network outside of Drosophila.


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