scholarly journals Gap genes are involved in inviability in hybrids between Drosophila melanogaster and D. santomea

2021 ◽  
Author(s):  
Wenhan Chang ◽  
Martin Kreitman ◽  
Daniel R. Matute
Keyword(s):  
Drosophila Melanogaster ◽  
Gene Network ◽  
Developmental Process ◽  
Coding Region ◽  
Pure Species ◽  
Closely Related Species ◽  
Hybrid Inviability ◽  
Gap Gene ◽  
Gap Genes ◽  
Anterior Posterior

ABSTRACTEvolved changes within species lead to the inevitable loss of viability in hybrids. Inviability is also a convenient phenotype to genetically map and validate functionally divergent genes and pathways differentiating closely related species. Here we identify the Drosophila melanogaster form of the highly conserved essential gap gene giant (gt) as a key genetic determinant of hybrid inviability in crosses with D. santomea. We show that the coding region of this allele in D. melanogaster/D. santomea hybrids is sufficient to cause embryonic inviability not seen in either pure species. Further genetic analysis indicates that tailless (tll), another gap gene, is also involved in the hybrid defects. giant and tll are both members of the gap gene network of transcription factors that participate in establishing anterior-posterior specification of the dipteran embryo, a highly conserved developmental process. Genes whose outputs in this process are functionally conserved nevertheless evolve over short timescales to cause inviability in hybrids.

scholarly journals A re-inducible gap gene cascade patterns the anterior-posterior axis of insects in a threshold-free fashion

2018 ◽  
Author(s):  
Alena Boos ◽  
Jutta Distler ◽  
Heike Rudolf ◽  
Martin Klingler ◽  
Ezzat El-Sherif
Keyword(s):  
Gene Network ◽  
Hox Genes ◽  
Expression Patterns ◽  
Fruit Fly ◽  
Regulation Mechanism ◽  
Gap Gene ◽  
Speed Regulation ◽  
Gap Genes ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

AbstractGap genes mediate the division of the anterior-posterior axis of insects into different fates through regulating downstream hox genes. Decades of tinkering the segmentation gene network of the long-germ fruit fly Drosophila melanogaster led to the conclusion that gap genes are regulated (at least initially) through a threshold-based French Flag model, guided by both anteriorly- and posteriorly-localized morphogen gradients. In this paper, we show that the expression patterns of gap genes in the intermediate-germ beetle Tribolium castaneum are mediated by a threshold-free ‘Speed Regulation’ mechanism, in which the speed of a genetic cascade of gap genes is regulated by a posterior gradient of the transcription factor Caudal. We show this by re-inducing the leading gap gene (namely, hunchback) resulting in the re-induction of the gap gene cascade at arbitrary points in time. This demonstrates that the gap gene network is self-regulatory and is primarily under the control of a posterior speed regulator in Tribolium and possibly all insects.

scholarly journals A re-inducible gap gene cascade patterns the anterior–posterior axis of insects in a threshold-free fashion

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Alena Boos ◽  
Jutta Distler ◽  
Heike Rudolf ◽  
Martin Klingler ◽  
Ezzat El-Sherif
Keyword(s):  
Gene Network ◽  
Hox Genes ◽  
Morphogen Gradient ◽  
Regulation Mechanism ◽  
Morphogen Gradients ◽  
Gap Gene ◽  
Speed Regulation ◽  
Gap Genes ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

Gap genes mediate the division of the anterior-posterior axis of insects into different fates through regulating downstream hox genes. Decades of tinkering the segmentation gene network of Drosophila melanogaster led to the conclusion that gap genes are regulated (at least initially) through a threshold-based mechanism, guided by both anteriorly- and posteriorly-localized morphogen gradients. In this paper, we show that the response of the gap gene network in the beetle Tribolium castaneum upon perturbation is consistent with a threshold-free ‘Speed Regulation’ mechanism, in which the speed of a genetic cascade of gap genes is regulated by a posterior morphogen gradient. We show this by re-inducing the leading gap gene (namely, hunchback) resulting in the re-induction of the gap gene cascade at arbitrary points in time. This demonstrates that the gap gene network is self-regulatory and is primarily under the control of a posterior regulator in Tribolium and possibly other short/intermediate-germ insects.

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 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 Morphogenesis at criticality

2014 ◽  
Vol 111 (10) ◽  
pp. 3683-3688 ◽  
Author(s):  
Dmitry Krotov ◽  
Julien O. Dubuis ◽  
Thomas Gregor ◽  
William Bialek
Keyword(s):  
Transcription Factors ◽  
Spatial Patterns ◽  
Gaussian Distribution ◽  
Gene Network ◽  
Fruit Fly ◽  
Genetic Network ◽  
Strong Correlations ◽  
Expression Levels ◽  
Gap Gene ◽  
Gap Genes

Spatial patterns in the early fruit fly embryo emerge from a network of interactions among transcription factors, the gap genes, driven by maternal inputs. Such networks can exhibit many qualitatively different behaviors, separated by critical surfaces. At criticality, we should observe strong correlations in the fluctuations of different genes around their mean expression levels, a slowing of the dynamics along some but not all directions in the space of possible expression levels, correlations of expression fluctuations over long distances in the embryo, and departures from a Gaussian distribution of these fluctuations. Analysis of recent experiments on the gap gene network shows that all these signatures are observed, and that the different signatures are related in ways predicted by theory. Although there might be other explanations for these individual phenomena, the confluence of evidence suggests that this genetic network is tuned to criticality.

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.

scholarly journals An efficient gene regulatory network inference algorithm for early Drosophila melanogaster embryogenesis

2017 ◽  
Author(s):  
Hirotaka Matsumoto ◽  
Hisanori Kiryu ◽  
Yasuhiro Kojima ◽  
Suguru Yaginuma ◽  
Itoshi Nikaido
Keyword(s):  
Drosophila Melanogaster ◽  
Regulatory Network ◽  
Efficient Algorithm ◽  
Large Scale ◽  
Gap Gene ◽  
Large Scale Data ◽  
Gap Genes ◽  
Simulation Based ◽  
Gene Regulatory ◽  
Scale Data

AbstractThe spatial patterns of gene expression in early Drosophila melanogaster embryogenesis have been studied experimentally and theoretically to reveal the molecular basis of morphogenesis. In particular, the gene regulatory network (GRN) of gap genes has been investigated through mathematical modeling and simulation. Although these simulation-based approaches are useful for describing complex dynamics and have revealed several important regulations in spatial patterning, they are computationally intensive because they optimize GRN with iterative simulation. Recently, the advance of experimental technologies is enabling the acquisition of comprehensive spatial expression data, and an efficient algorithm will be necessary to analyze such large-scale data. In this research, we developed an efficient algorithm to infer the GRN based on a linear reaction-diffusion model. First, we qualitatively analyzed the GRNs of gap genes and pair-rule genes based on our algorithm and showed that two mutual repressions are fundamental regulations. Then, we inferred the GRN from gap gene data, and identified asymmetric regulations in addition to the two mutual repressions. We analyzed the effect of these asymmetric regulations on spatial patterns, and showed that they have the potential to adjust peak position. Our algorithm runs in sub-second time, which is significantly smaller than the runtime of simulation-based approaches (between 8 and 160 h, for exmaple). Neverthe-less, our inferred GRN was highly correlated with the simulation-based GRNs. We also analyzed the gap gene network of Clogmia albipunctata and showed that different mutual repression regulations might be important in comparison with those of Drosophila melanogaster. As our algorithm can infer GRNs efficiently and can be applied to several different network analysis, it will be a valuable approach for analyzing large-scale data.

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.

scholarly journals Reverse Engineering the Gap Gene Network of Drosophila melanogaster

2006 ◽  
Vol 2 (5) ◽  
pp. e51 ◽  
Author(s):  
Theodore J Perkins ◽  
Johannes Jaeger ◽  
John Reinitz ◽  
Leon Glass
Keyword(s):  
Drosophila Melanogaster ◽  
Reverse Engineering ◽  
Gene Network ◽  
Gap Gene

scholarly journals Dynamic Maternal Gradients Control Timing and Shift-Rates forDrosophilaGap Gene Expression

2016 ◽  
Author(s):  
Berta Verd ◽  
Anton Crombach ◽  
Johannes Jaeger
Keyword(s):  
Gene Expression ◽  
Gene Regulation ◽  
Drosophila Melanogaster ◽  
Pattern Formation ◽  
Dynamic Process ◽  
Gene Expression Pattern ◽  
The Body ◽  
Transient Dynamics ◽  
Gap Gene ◽  
Gap Genes

AbstractPattern formation during development is a highly dynamic process. In spite of this, few experimental and modelling approaches take into account the explicit time-dependence of the rules governing regulatory systems. We address this problem by studying dynamic morphogen interpretation by the gap gene network inDrosophila melanogaster. Gap genes are involved in segment determination during early embryogenesis. They are activated by maternal morphogen gradients encoded bybicoid (bcd)andcaudal (cad). These gradients decay at the same time-scale as the establishment of the antero-posterior gap gene pattern. We use a reverse-engineering approach, based on data-driven regulatory models called gene circuits, to isolate and characterise the explicitly time-dependent effects of changing morphogen concentrations on gap gene regulation. To achieve this, we simulate the system in the presence and absence of dynamic gradient decay. Comparison between these simulations reveals that maternal morphogen decay controls the timing and limits the rate of gap gene expression. In the anterior of the embyro, it affects peak expression and leads to the establishment of smooth spatial boundaries between gap domains. In the posterior of the embryo, it causes a progressive slow-down in the rate of gap domain shifts, which is necessary to correctly position domain boundaries and to stabilise the spatial gap gene expression pattern. We use a newly developed method for the analysis of transient dynamics in non-autonomous (time-variable) systems to understand the regulatory causes of these effects. By providing a rigorous mechanistic explanation for the role of maternal gradient decay in gap gene regulation, our study demonstrates that such analyses are feasible and reveal important aspects of dynamic gene regulation which would have been missed by a traditional steady-state approach. More generally, it highlights the importance of transient dynamics for understanding complex regulatory processes in development.Author SummaryAnimal development is a highly dynamic process. Biochemical or environmental signals can cause the rules that shape it to change over time. We know little about the effects of such changes. For the sake of simplicity, we usually leave them out of our models and experimental assays. Here, we do exactly the opposite. We characterise precisely those aspects of pattern formation caused by changing signalling inputs to a gene regulatory network, the gap gene system ofDrosophila melanogaster. Gap genes are involved in determining the body segments of flies and other insects during early development. Gradients of maternal morphogens activate the expression of the gap genes. These gradients are highly dynamic themselves, as they decay while being read out. We show that this decay controls the peak concentration of gap gene products, produces smooth boundaries of gene expression, and slows down the observed positional shifts of gap domains in the posterior of the embryo, thereby stabilising the spatial pattern. Our analysis demonstrates that the dynamics of gene regulation not only affect the timing, but also the positioning of gene expression. This suggests that we must pay closer attention to transient dynamic aspects of development than is currently the case.

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