scholarly journals Quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly Megaselia abdita

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Karl R Wotton ◽  
Eva Jiménez-Guri ◽  
Anton Crombach ◽  
Hilde Janssens ◽  
Anna Alcaine-Colet ◽  
...  
Keyword(s):  
Gene Expression ◽  
Gene Network ◽  
Mechanistic Explanation ◽  
Developmental Evolution ◽  
Gap Gene ◽  
Spatio Temporal ◽  
Mechanistic Basis ◽  
Hourglass Model ◽  
Network Rewiring ◽  
Megaselia Abdita

The segmentation gene network in insects can produce equivalent phenotypic outputs despite differences in upstream regulatory inputs between species. We investigate the mechanistic basis of this phenomenon through a systems-level analysis of the gap gene network in the scuttle fly Megaselia abdita (Phoridae). It combines quantification of gene expression at high spatio-temporal resolution with systematic knock-downs by RNA interference (RNAi). Initiation and dynamics of gap gene expression differ markedly between M. abdita and Drosophila melanogaster, while the output of the system converges to equivalent patterns at the end of the blastoderm stage. Although the qualitative structure of the gap gene network is conserved, there are differences in the strength of regulatory interactions between species. We term such network rewiring ‘quantitative system drift’. It provides a mechanistic explanation for the developmental hourglass model in the dipteran lineage. Quantitative system drift is likely to be a widespread mechanism for developmental evolution.

scholarly journals Gene Expression Does Not Support the Developmental Hourglass Model in Three Animals with Spiralian Development

2019 ◽  
Vol 36 (7) ◽  
pp. 1373-1383 ◽  
Author(s):  
Longjun Wu ◽  
Kailey E Ferger ◽  
J David Lambert
Keyword(s):  
Gene Expression ◽  
Large Fraction ◽  
Molecular Data ◽  
Development Stage ◽  
Data Sets ◽  
Rna Seq ◽  
Developmental Evolution ◽  
Phylotypic Stage ◽  
Hourglass Model ◽  
Almost All

Abstract It has been proposed that animals have a pattern of developmental evolution resembling an hourglass because the most conserved development stage—often called the phylotypic stage—is always in midembryonic development. Although the topic has been debated for decades, recent studies using molecular data such as RNA-seq gene expression data sets have largely supported the existence of periods of relative evolutionary conservation in middevelopment, consistent with the phylotypic stage and the hourglass concepts. However, so far this approach has only been applied to a limited number of taxa across the tree of life. Here, using established phylotranscriptomic approaches, we found a surprising reverse hourglass pattern in two molluscs and a polychaete annelid, representatives of the Spiralia, an understudied group that contains a large fraction of metazoan body plan diversity. These results suggest that spiralians have a divergent midembryonic stage, with more conserved early and late development, which is the inverse of the pattern seen in almost all other organisms where these phylotranscriptomic approaches have been reported. We discuss our findings in light of proposed reasons for the phylotypic stage and hourglass model in other systems.

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 Author response: Quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly Megaselia abdita

2014 ◽  
Author(s):  
Karl R Wotton ◽  
Eva Jiménez-Guri ◽  
Anton Crombach ◽  
Hilde Janssens ◽  
Anna Alcaine-Colet ◽  
...  
Keyword(s):  
Gene Network ◽  
Author Response ◽  
Gap Gene ◽  
Megaselia Abdita

scholarly journals Sequence-based model of gap gene regulatory network

2015 ◽  
Author(s):  
Konstantin N Kozlov ◽  
Vitaly V Gursky ◽  
Ivan V Kulakovskiy ◽  
Maria G Samsonova
Keyword(s):  
Gene Expression ◽  
Transcription Factor ◽  
Binding Sites ◽  
Gene Network ◽  
Expression Patterns ◽  
Gene Expression Patterns ◽  
Model Output ◽  
Wild Type ◽  
Gap Gene ◽  
Gene Regulatory

Background: The detailed analysis of transcriptional regulation is crucially important for understanding biological processes. The gap gene network in Drosophila attracts large interest among researches studying mechanisms of transcriptional regulation. It implements the most upstream regulatory layer of the segmentation gene network. The knowledge of molecular mechanisms involved in gap gene regulation is far less complete than that of genetics of the system. Mathematical modeling goes beyond insights gained by genetics and molecular approaches. It allows us to reconstruct wild-type gene expression patterns in silico, infer underlying regulatory mechanism and prove its sufficiency. Results: We developed a new model that provides a dynamical description of gap gene regulatory systems, using detailed DNA-based information, as well as spatial transcription factor concentration data at varying time points. We showed that this model correctly reproduces gap gene expression patterns in wild type embryos and is able to predict gap expression patterns in Kr mutants and four reporter constructs. We used four-fold cross validation test and fitting to random dataset to validate the model and proof its sufficiency in data description. The identifiability analysis showed that most model parameters are well identifiable. We reconstructed the gap gene network topology and studied the impact of individual transcription factor binding sites on the model output. We measured this impact by calculating the site regulatory weight as a normalized difference between the residual sum of squares error for the set of all annotated sites and the set, from which the site of interest was left out. Conclusions: The reconstructed topology of the gap gene network is in agreement with previous modeling results and data from literature. We showed that 1) the regulatory weights of transcription factor binding sites show very weak correlation with their PWM score; 2) sites with low regulatory weight are important for the model output; 3) functional important sites are not exclusively located in cis-regulatory elements, but are rather dispersed through regulatory region. It is of importance that some of the sites with high functional impact in hb, Kr and kni regulatory regions coincide with strong sites annotated and verified in Dnase I footprint assays. Keywords: transcription; thermodynamics; reaction-diffusion; drosophila

scholarly journals Binary Expression Enhances Reliability of Messaging in Gene Networks

Entropy ◽  
2020 ◽  
Vol 22 (4) ◽  
pp. 479
Author(s):  
Leonardo R. Gama ◽  
Guilherme Giovanini ◽  
Gábor Balázsi ◽  
Alexandre F. Ramos
Keyword(s):  
Gene Expression ◽  
Transcription Factors ◽  
Mutual Information ◽  
Gene Networks ◽  
Gene Network ◽  
The State ◽  
Expression Levels ◽  
Temporal Precision ◽  
Spatio Temporal ◽  
Steady State Solutions

The promoter state of a gene and its expression levels are modulated by the amounts of transcription factors interacting with its regulatory regions. Hence, one may interpret a gene network as a communicating system in which the state of the promoter of a gene (the source) is communicated by the amounts of transcription factors that it expresses (the message) to modulate the state of the promoter and expression levels of another gene (the receptor). The reliability of the gene network dynamics can be quantified by Shannon’s entropy of the message and the mutual information between the message and the promoter state. Here we consider a stochastic model for a binary gene and use its exact steady state solutions to calculate the entropy and mutual information. We show that a slow switching promoter with long and equally standing ON and OFF states maximizes the mutual information and reduces entropy. That is a binary gene expression regime generating a high variance message governed by a bimodal probability distribution with peaks of the same height. Our results indicate that Shannon’s theory can be a powerful framework for understanding how bursty gene expression conciliates with the striking spatio-temporal precision exhibited in pattern formation of developing organisms.

scholarly journals Gap gene regulatory dynamics evolve along a genotype network

2015 ◽  
Author(s):  
Anton Crombach ◽  
Karl R Wotton ◽  
Eva Jimenez-Guri ◽  
Johannes Jaeger
Keyword(s):  
Gene Expression ◽  
Gene Networks ◽  
Regulatory Networks ◽  
Model Organism ◽  
Regulatory Mechanisms ◽  
Gap Gene ◽  
Modeling Analysis ◽  
Regulatory Dynamics ◽  
Gene Regulatory ◽  
Megaselia Abdita

Developmental gene networks implement the dynamic regulatory mechanisms that pattern and shape the organism. Over evolutionary time, the wiring of these networks changes, yet the patterning outcome is often preserved, a phenomenon known as “system drift”. System drift is illustrated by the gap gene network—involved in segmental patterning—in dipteran insects. In the classic model organismDrosophila melanogasterand the non-model scuttle flyMegaselia abdita, early activation and placement of gap gene expression domains show significant quantitative differences, yet the final patterning output of the system is essentially identical in both species. In this detailed modeling analysis of system drift, we use gene circuits which are fit to quantitative gap gene expression data inM. abditaand compare them to an equivalent set of models fromD. melanogaster. The results of this comparative analysis show precisely how compensatory regulatory mechanisms achieve equivalent final patterns in both species. We discuss the larger implications of the work in terms of “genotype networks” and the ways in which the structure of regulatory networks can influence patterns of evolutionary change (evolvability).

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

Development ◽  
2021 ◽  
Author(s):  
Olivia RA Tidswell ◽  
Matthew A. Benton ◽  
Michael Akam
Keyword(s):  
Gene Expression ◽  
Stem Cells ◽  
Neural Stem Cells ◽  
Crucial Role ◽  
Gene Network ◽  
Homeotic Transformation ◽  
Hox Gene ◽  
Gap Gene ◽  
Gap Genes ◽  
And Function

The neuroblast timer genes hunchback, Krüppel, nubbin, and castor are expressed in temporal sequence in neural stem cells, and in corresponding spatial sequence along the Drosophila blastoderm. As canonical gap genes, hunchback and Krüppel play a crucial role in insect segmentation, but the roles of nubbin and castor in this process remain ambiguous. We have investigated the expression and functions of nubbin and castor during segmentation in the beetle Tribolium. We show that Tc-hunchback, Tc-Krüppel, Tc-nubbin and Tc-castor are expressed sequentially in the segment addition zone, and that Tc-nubbin regulates segment identity redundantly with two previously described gap/gap-like genes, Tc-giant and Tc-knirps. Simultaneous knockdown of Tc-nubbin, Tc-giant and Tc-knirps results in the formation of ectopic legs on abdominal segments. 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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