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 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 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 Hox genes are essential for the development of eyespots in Bicyclus anynana butterflies

Genetics ◽  
2020 ◽  
Vol 217 (1) ◽  
Author(s):  
Yuji Matsuoka ◽  
Antónia Monteiro
Keyword(s):  
Hox Genes ◽  
Bicyclus Anynana ◽  
Hox Gene ◽  
Novel Traits ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

Abstract The eyespot patterns found on the wings of nymphalid butterflies are novel traits that originated first in hindwings and subsequently in forewings, suggesting that eyespot development might be dependent on Hox genes. Hindwings differ from forewings in the expression of Ultrabithorax (Ubx), but the function of this Hox gene in eyespot development as well as that of another Hox gene Antennapedia (Antp), expressed specifically in eyespots centers on both wings, are still unclear. We used CRISPR-Cas9 to target both genes in Bicyclus anynana butterflies. We show that Antp is essential for eyespot development on the forewings and for the differentiation of white centers and larger eyespots on hindwings, whereas Ubx is essential not only for the development of at least some hindwing eyespots but also for repressing the size of other eyespots. Additionally, Antp is essential for the development of silver scales in male wings. In summary, Antp and Ubx, in addition to their conserved roles in modifying serially homologous segments along the anterior–posterior axis of insects, have acquired a novel role in promoting the development of a new set of serial homologs, the eyespot patterns, in both forewings (Antp) and hindwings (Antp and Ubx) of B. anynana butterflies. We propose that the peculiar pattern of eyespot origins on hindwings first, followed by forewings, could be due to an initial co-option of Ubx into eyespot development followed by a later, partially redundant, co-option of Antp into the same network.

Hox genes and the evolution of vertebrate axial morphology

Development ◽  
1995 ◽  
Vol 121 (2) ◽  
pp. 333-346 ◽  
Author(s):  
A.C. Burke ◽  
C.E. Nelson ◽  
B.A. Morgan ◽  
C. Tabin
Keyword(s):  
Hox Genes ◽  
Cervical Vertebrae ◽  
Homeobox Gene ◽  
Paraxial Mesoderm ◽  
Thoracic Vertebrae ◽  
Homeotic Genes ◽  
Evolutionary Variation ◽  
Axial Morphology ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

A common form of evolutionary variation between vertebrate taxa is the different numbers of segments that contribute to various regions of the anterior-posterior axis; cervical vertebrae, thoracic vertebrae, etc. The term ‘transposition’ is used to describe this phenomenon. Genetic experiments with homeotic genes in mice have demonstrated that Hox genes are in part responsible for the specification of segmental identity along the anterior-posterior axis, and it has been proposed that an axial Hox code determines the morphology of individual vertebrae (Kessel, M. and Gruss, P. (1990) Science 249, 347–379). This paper presents a comparative study of the developmental patterns of homeobox gene expression and developmental morphology between animals that have homologous regulatory genes but different morphologies. The axial expression boundaries of 23 Hox genes were examined in the paraxial mesoderm of chick, and 16 in mouse embryos by in situ hybridization and immunolocalization techniques. Hox gene anterior expression boundaries were found to be transposed in concert with morphological boundaries. This data contributes a mechanistic level to the assumed homology of these regions in vertebrates. The recognition of mechanistic homology supports the historical homology of basic patterning mechanisms between all organisms that share these genes.

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 Disappearance of Temporal Collinearity in Vertebrates and its Eventual Reappearance

2021 ◽  
Author(s):  
Spyros Papageorgiou
Keyword(s):  
Hox Genes ◽  
Hox Cluster ◽  
Spatial Dimensions ◽  
Anterior Posterior ◽  
As If ◽  
Anterior Posterior Axis

It was observed that a cluster of ordered genes (Hox1, Hox2, Hox3,…) in the genome are activated in the ontogenetic units (1, 2, 3,…) of an embryo along the Anterior/Posterior axis following the same order of the Hox genes. This Spatial Collinearity (SC) is very strange since it correlates events of very different spatial dimensions. It was later observed in vertebrates, that, in the above ordering, first is Hox1expressed in ontogenetic unit 1, followed later by Hox2 in unit 2, and even later Hox3 in unit 3….This temporal collinearity (TC) is an enigma and even to-day is explored in depth. In 1999 T. Kondo and D. Duboule, after posterior upstream extended DNA excisions , concluded that the Hox cluster behaves ‘as if’ TC disappears. Here the consideration of TC really disappearing is taken face value and its repercussions are analyzed. Furthermore, an experiment is proposed to test TC disappearance. An outcome of this experiment could be the reappearance (partial or total) of TC.

scholarly journals Hox genes are essential for the development of novel serial homologous eyespots on the wings of Bicyclus anynana butterflies

2019 ◽  
Author(s):  
Yuji Matsuoka ◽  
Antónia Monteiro
Keyword(s):  
Hox Genes ◽  
Bicyclus Anynana ◽  
Hox Gene ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

AbstractThe eyespot patterns found on the wings of nymphalid butterflies are novel serial homologous traits that originated first in hindwings and subsequently in forewings, suggesting that eyespot development might be dependent on Hox genes. Hindwings differ from forewings in the expression of Ultrabithorax (Ubx), but the function of this Hox gene in eyespot development as well as that of another Hox gene Antennapedia (Antp), expressed specifically in eyespots centers on both wings, are still unclear. We used CRISPR-Cas9 to target both genes in Bicyclus anynana butterflies. We show that Antp is essential for eyespot development on the forewings and for the differentiation of white centers and larger eyespots on hindwings, whereas Ubx is essential for the development of at least some hindwing eyespots but also for repressing the size of other eyespots. Additionally, Antp is essential for the development of silver scales in male wings. In summary, Antp and Ubx, in addition to their conserved roles in modifying serial homologous traits along the anterior-posterior axis of animals, have acquired a novel role in promoting the development of a new set of serial homologs, the eyespot patterns, in both forewings (Antp) and hindwings (Antp and Ubx) of B. anynana butterflies. We propose that the peculiar pattern of eyespot origins on hindwings first, followed by forewings, could be due to an initial co-option of Ubx into eyespot development, followed by a later, partially redundant co-option of Antp into the same network.

Sign in / Sign up

Export Citation Format

Share Document