scholarly journals Dual mode of embryonic development is highlighted by expression and function of Nasonia pair-rule genes

eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Miriam I Rosenberg ◽  
Ava E Brent ◽  
François Payre ◽  
Claude Desplan
Keyword(s):  
Gene Expression ◽  
Embryonic Development ◽  
Mixed Mode ◽  
Complete Loss ◽  
Dual Mode ◽  
Gap Gene ◽  
And Function ◽  
Pair Rule ◽  
Anterior Posterior

Embryonic anterior–posterior patterning is well understood in Drosophila, which uses ‘long germ’ embryogenesis, in which all segments are patterned before cellularization. In contrast, most insects use ‘short germ’ embryogenesis, wherein only head and thorax are patterned in a syncytial environment while the remainder of the embryo is generated after cellularization. We use the wasp Nasonia (Nv) to address how the transition from short to long germ embryogenesis occurred. Maternal and gap gene expression in Nasonia suggest long germ embryogenesis. However, the Nasonia pair-rule genes even-skipped, odd-skipped, runt and hairy are all expressed as early blastoderm pair-rule stripes and late-forming posterior stripes. Knockdown of Nv eve, odd or h causes loss of alternate segments at the anterior and complete loss of abdominal segments. We propose that Nasonia uses a mixed mode of segmentation wherein pair-rule genes pattern the embryo in a manner resembling Drosophila at the anterior and ancestral Tribolium at the posterior.

scholarly journals Conservation and variation in pair-rule gene expression and function in the intermediate-germ beetleDermestes maculatus

Development ◽  
2017 ◽  
Vol 144 (24) ◽  
pp. 4625-4636 ◽  
Author(s):  
Jie Xiang ◽  
Katie Reding ◽  
Alison Heffer ◽  
Leslie Pick
Keyword(s):  
Gene Expression ◽  
Pair Rule Gene ◽  
And Function ◽  
Pair Rule

scholarly journals The neuroblast timer gene nubbin exhibits functional redundancy with gap genes to regulate segment identity in Tribolium

2021 ◽  
Author(s):  
Olivia R A Tidswell ◽  
Matthew A Benton ◽  
Michael E Akam
Keyword(s):  
Gene Expression ◽  
Regulatory Network ◽  
Gene Network ◽  
In Situ Hybridisation ◽  
Hox Gene ◽  
Gap Gene ◽  
Gap Genes ◽  
Sequential Mode ◽  
And Function

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.

scholarly journals Embryonic geometry underlies phenotypic variation in decanalized conditions

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Anqi Huang ◽  
Jean-François Rupprecht ◽  
Timothy E Saunders
Keyword(s):  
Gene Expression ◽  
Aspect Ratio ◽  
Phenotypic Variation ◽  
Drosophila Embryo ◽  
Wild Type ◽  
Gap Gene ◽  
Key Factor ◽  
Segmentation Gene Expression ◽  
Environmental Variations ◽  
Anterior Posterior

During development, many mutations cause increased variation in phenotypic outcomes, a phenomenon termed decanalization. Phenotypic discordance is often observed in the absence of genetic and environmental variations, but the mechanisms underlying such inter-individual phenotypic discordance remain elusive. Here, using the anterior-posterior (AP) patterning of the Drosophila embryo, we identified embryonic geometry as a key factor predetermining patterning outcomes under decanalizing mutations. With the wild-type AP patterning network, we found that AP patterning is robust to variations in embryonic geometry; segmentation gene expression remains reproducible even when the embryo aspect ratio is artificially reduced by more than twofold. In contrast, embryonic geometry is highly predictive of individual patterning defects under decanalized conditions of either increased bicoid (bcd) dosage or bcd knockout. We showed that the phenotypic discordance can be traced back to variations in the gap gene expression, which is rendered sensitive to the geometry of the embryo under mutations.

scholarly journals Speeding up anterior-posterior patterning of insects by differential initialization of the gap gene cascade

2018 ◽  
Author(s):  
Heike Rudolf ◽  
Christine Zellner ◽  
Ezzat El-Sherif
Keyword(s):  
Gene Expression ◽  
Drosophila Melanogaster ◽  
Fruit Fly ◽  
Red Flour Beetle ◽  
Evolutionary Transition ◽  
Gap Gene ◽  
Sequential Mode ◽  
Patterning Genes ◽  
Computational Analyses ◽  
Anterior Posterior

AbstractRecently, it was shown that anterior-posterior patterning genes in the red flour beetle Tribolium castaneum are expressed sequentially in waves. However, in the fruit fly Drosophila melanogaster, an insect with a derived mode of embryogenesis compared to Tribolium, anterior-posterior patterning genes quickly and simultaneously arise as mature gene expression domains that, afterwards, undergo slight posterior-to-anterior shifts. This raises the question of how a fast and simultaneous mode of patterning, like that of Drosophila, could have evolved from a rather slow sequential mode of patterning, like that of Tribolium. In this paper, we elucidate a mechanism for this evolutionary transition based on a switch from a uniform to a gradient-mediated initialization of the gap gene cascade by maternal Hb. The model is supported by computational analyses and experiments.

The zygotic control of Drosophila pair-rule gene expression. II. Spatial repression by gap and pair-rule gene products

Development ◽  
1989 ◽  
Vol 107 (3) ◽  
pp. 673-683 ◽  
Author(s):  
S.B. Carroll ◽  
S.H. Vavra
Keyword(s):  
Gene Expression ◽  
Expression Patterns ◽  
Control Mechanisms ◽  
Gap Gene ◽  
Gap Genes ◽  
Gene Mutant ◽  
Pair Rule Gene ◽  
Regulatory Effects ◽  
Pair Rule ◽  
Zygotic Control

We examined gene expression patterns in certain single and double pair-rule mutant embryos to determine which of the largely repressive pair-rule gene interactions are most likely to be direct and which interactions are probably indirect. From these studies we conclude that: (i) hairy+ and even-skipped (eve+) regulate the fushi tarazu (ftz) gene; (ii) eve+ and runt+ regulate the hairy gene; (iii) runt+ regulates the eve gene; but, (iv) runt does not regulate the ftz gene pattern, and hairy does not regulate the eve gene pattern. These pair-rule interactions are not sufficient, however, to explain the periodicity of the hairy and eve patterns, so we examined specific gap gene mutant combinations to uncover their regulatory effects on these two genes. Our surprising observation is that the hairy and eve genes are expressed in embryos where the three key gap genes hunchback (hb), Kruppel (Kr), and knirps (kni) have been removed, indicating that these gap genes are not essential to activate the pair-rule genes. In fact, we show that in the absence of either hb+ or kni+, or both gap genes, the Kr+ product represses hairy expression. These results suggest that gap genes repress hairy expression in the interstripe regions, rather than activate hairy expression in the stripes. The molecular basis of pair-rule gene regulation by gap genes must involve some dual control mechanisms such that combinations of gap genes affect pair-rule transcription in a different manner than a single gap gene.

Analysis of maternal effect mutant combinations elucidates regulation and function of the overlap of hunchback and Kruppel gene expression in the Drosophila blastoderm embryo

Development ◽  
1989 ◽  
Vol 107 (3) ◽  
pp. 651-662 ◽  
Author(s):  
U. Gaul ◽  
H. Jackle
Keyword(s):  
Maternal Effect ◽  
Drosophila Embryo ◽  
Homeotic Genes ◽  
Protein Distribution ◽  
Wild Type ◽  
Gap Gene ◽  
Gap Genes ◽  
Underlying Mechanisms ◽  
And Function ◽  
Pair Rule

The metameric organisation of the Drosophila embryo is generated early during development, due to the action of maternal effect and zygotic segmentation and homeotic genes. The gap genes participate in the complex process of pattern formation by providing a link between the maternal and the zygotic gene activities. Under the influence of maternal gene products they become expressed in distinct domains along the anteroposterior axis of the embryo; negative interactions between neighboring gap genes are thought to be involved in establishing the expression domains. The gap gene activities in turn are required for the correct patterning of the pair-rule genes; little is known, however, about the underlying mechanisms. We have monitored the distribution of gap and pair-rule genes in wild-type embryos and in embryos in which the anteroposterior body pattern is greatly simplified due to combinations of maternal effect mutations (staufen exuperantia, vasa exuperantia, vasa exuperantia, bicoid oskar, bicoid oskar torsolike, vasa torso exuperantia). We show that the domains of protein distribution of the gap genes hunchback and Kruppel overlap in wild-type embryos. Based on the analysis of the maternal mutant combinations, we suggest an explanation of how this overlap is generated. Furthermore, our data show that different constellations of gap gene activities provide different input for the pair-rule genes, and thus strongly suggest that the overlap of hunchback and Kruppel in wild-type is functional in the formation of the patterns of pair-rule genes.

scholarly journals Evidence for the temporal regulation of insect segmentation by a conserved set of developmental transcription factors

2017 ◽  
Author(s):  
Erik Clark ◽  
Andrew D. Peel
Keyword(s):  
Gene Expression ◽  
Drosophila Melanogaster ◽  
Transcription Factors ◽  
Tribolium Castaneum ◽  
Fruit Fly ◽  
Temporal Regulation ◽  
Gap Gene ◽  
Spatiotemporal Information ◽  
Segmentation Gene Expression ◽  
Pair Rule

ABSTRACTLong-germ insects, such as the fruit fly Drosophila melanogaster, pattern their segments simultaneously, whereas short germ insects, such as the beetle Tribolium castaneum, pattern their segments sequentially, from anterior to posterior. While the two modes of segmentation at first appear to be very different, many details of segmentation gene expression are surprisingly similar between long-germ and short-germ species. Collectively, these observations hint that insect segmentation may involve fairly conserved patterning mechanisms, which occur within an evolutionarily malleable spatiotemporal framework. Based on genetic and comparative evidence, we now propose that, in both Drosophila and Tribolium embryos, the temporal progression of the segmentation process is regulated by a temporal sequence of Caudal, Dichaete, and Odd-paired expression. These three transcription factors are broadly expressed in segmenting tissues, providing spatiotemporal information that intersects with the information provided by periodically-expressed segmentation genes such as the pair-rule factors. However, they are deployed differently in long-germ versus short-germ insects, acting as simple timers in Drosophila, but as smooth, retracting wavefronts in Tribolium, compatible with either gap gene-based or oscillator-based generation of periodicity, respectively.

Interactions of the Drosophila gap gene giant with maternal and zygotic pattern-forming genes

Development ◽  
1991 ◽  
Vol 111 (2) ◽  
pp. 367-378 ◽  
Author(s):  
E.D. Eldon ◽  
V. Pirrotta
Keyword(s):  
Gene Expression ◽  
Embryonic Development ◽  
Nuclear Protein ◽  
The Other ◽  
Head Region ◽  
Gap Gene ◽  
Gap Genes ◽  
Ring Gland ◽  
Pattern Forming ◽  
Initial Pattern

The Drosophila gene giant (gt) is a segmentation gene that affects anterior head structures and abdominal segments A5-A7. Immunolocalization of the gt product shows that it is a nuclear protein whose expression is initially activated in an anterior and a posterior domain. Activation of the anterior domain is dependent on the maternal bicoid gradient while activation of the posterior domain requires maternal nanos gene product. Initial expression is not abolished by mutations in any of the zygotic gap genes. By cellular blastoderm, the initial pattern of expression has evolved into one posterior and three anterior stripes of expression. The evolution, position and width of these stripes are dependent on interactions between gt and the other gap genes. In turn, gt activity in these domains affects the expression of the other gap genes. These interactions, typical of the cross-regulation previously observed among gap genes, confirm that gt is a member of the gap gene class whose function is necessary to establish the overall pattern of gap gene expression. After cellular blastoderm, gt protein continues to be expressed in the head region in parts of the maxillary and mandibular segments as well as in the labrum. Expression is never detected in the labial or thoracic segment primordia but persists in certain head structures, including the ring gland, until the end of embryonic development.

Sign in / Sign up

Export Citation Format

Share Document