Time and space in segmentation

Clark, Erik

doi:10.1098/rsfs.2020.0049

Cited by 12 publications

(9 citation statements)

References 281 publications

(440 reference statements)

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“…If we modify the Drosophila timer gene network to incorporate these additional features (Appendix 4), we can see how appropriate segment addition zone dynamics might naturally emerge (Figure 8—figure Supplement 1). It therefore seems plausible that the cross-regulatory interactions between the Drosophila timer genes may represent an evolutionary vestige of a “dynamical module” that was originally involved in axial elongation (Clark and Peel, 2018; Clark, 2021). Functional experiments in sequentially segmenting species will be necessary to test this hypothesis.…”

Section: Discussionmentioning

confidence: 99%

“…In Supplementary Figure 26, the AP axis of a sequentially segmenting species is modelled as a growing array of "cells" with a Wg signalling centre at the posterior end, as in Clark, 2021. The domain starts at one cell long at t0, then adds a cell each iteration by duplicating the most posterior cell. The range of effective Wg signalling is finite (in this case, 8 cells from the posterior signalling centre), so the zone of Wg signalling moves posteriorly with time.…”

Section: Model Detailsmentioning

confidence: 99%

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A timer gene network is spatially regulated by the terminal system in theDrosophilaembryo

Clark

Battistara

Benton

2022

Preprint

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In insects, patterning of the anteroposterior axis relies on exquisite coordination of segmentation gene expression in space and time. And yet, there is also wide variation across species in the timing of segmentation and the geometry of the embryonic fate map. The majority of described species exhibit sequential segmentation during posterior growth. Other species, such as the fly Drosophila melanogaster, specify almost all of their segments simultaneously prior to gastrulation. The dynamics of both sequential segmentation and simultaneous segmentation correlate with the spatiotemporal expression of the "timer" genes caudal, Dichaete and odd-paired, which are expressed sequentially within segmenting tissues. These genes have critical roles in the development of many species; however, even in the extensively studied Drosophila embryo, the regulatory interactions responsible for shaping their expression remain poorly understood. In particular, it is not known whether the timer genes cross-regulate each other, nor why they are differentially expressed between the broad region of the blastoderm that gives rise to the gnathal, thoracic and abdominal segments and the small posterior region that gives rise to the embryonic terminalia. In this work, we investigated these questions using multiplexed fluorescent in situ hybridisation and high resolution confocal imaging of wild-type and mutant Drosophila embryos. First, we re-examined segmentation gene expression in the posterior of the embryo, and discovered that two parasegment-like boundaries are generated sequentially from the terminal region during germband extension and posterior growth. Next, we found that caudal, Dichaete, and odd-paired dynamically cross-regulate each other, and also that they are differentially spatially regulated by the posterior terminal genes. Finally, we formalised the regulatory network we inferred from our data as a logical computational model. Our model qualitatively recapitulated both wild-type development and the mutant phenotypes we had examined. Our findings resolve a decades-long ambiguity over the number of segments formed during Drosophila embryogenesis. In addition, they reveal how dynamic spatial inputs from an extrinsic signalling centre modulate the intrinsic dynamics of a gene regulatory network to generate an essential developmental pattern.

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Section: Discussionmentioning

confidence: 99%

Section: Model Detailsmentioning

confidence: 99%

A timer gene network is spatially regulated by the terminal system in theDrosophilaembryo

Clark

Battistara

Benton

2022

Preprint

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“…Recently, Clark and Peel (2018) proposed that in the SAZ, Wnt signaling would be regulating an ancient regulatory network formed by caudal, dichaete, and odd-paired (opa), which are sequentially expressed-both temporally and spatially-during segmentation in Tribolium, but also in the long-germ Drosophila embryo. Furthermore, one of the same authors proposed a transition from the posterior expression of caudal/ dichaete to dichaete/opa expression at the anterior region of the SAZ, resembling the wavefront limit operating in vertebrates (Clark, 2021). Then it is possible that the Wnt pathway is regulating, through Caudal, genetic oscillations in arthropods, as occurs in vertebrates.…”

Section: Wnt Signaling As Part Of the Genetic Network Underlying Segm...mentioning

confidence: 98%

The organizing role of Wnt signaling pathway during arthropod posterior growth

Mundaca-Escobar

Cepeda

Sarrazin

2022

Front. Cell Dev. Biol.

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Wnt signaling pathways are recognized for having major roles in tissue patterning and cell proliferation. In the last years, remarkable progress has been made in elucidating the molecular and cellular mechanisms that underlie sequential segmentation and axial elongation in various arthropods, and the canonical Wnt pathway has emerged as an essential factor in these processes. Here we review, with a comparative perspective, the current evidence concerning the participation of this pathway during posterior growth, its degree of conservation among the different subphyla within Arthropoda and its relationship with the rest of the gene regulatory network involved. Furthermore, we discuss how this signaling pathway could regulate segmentation to establish this repetitive pattern and, at the same time, probably modulate different cellular processes precisely coupled to axial elongation. Based on the information collected, we suggest that this pathway plays an organizing role in the formation of the body segments through the regulation of the dynamic expression of segmentation genes, via controlling the caudal gene, at the posterior region of the embryo/larva, that is necessary for the correct sequential formation of body segments in most arthropods and possibly in their common segmented ancestor. On the other hand, there is insufficient evidence to link this pathway to axial elongation by controlling its main cellular processes, such as convergent extension and cell proliferation. However, conclusions are premature until more studies incorporating diverse arthropods are carried out.

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“…A greater degree of hierarchical control is thereby imposed over what was previously, in more basal arthropods, a self-organizing process of sequential segmentation relying, as in vertebrates, on molecular clocks and moving wavefronts ( Salazar-Ciudad et al, 2001 ; Pourquié, 2003 ; Hunding and Baumgartner, 2017 ). A sequential mode of segmentation is characteristic of basal arthropods and short germ band insects like the beetle Tribolium , and there are plausible scenarios for linking this to the Drosophila condition through a complicated series of transitional steps ( Clark et al, 2019 ; Clark, 2021 ). If there is elegance here, it is well hidden.…”

Section: Flexibility In Pattern Selection: Spots Stripes and In-betweenmentioning

confidence: 99%

Patterning, From Conifers to Consciousness: Turing’s Theory and Order From Fluctuations

Lacalli

2022

Front. Cell Dev. Biol.

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This is a brief account of Turing’s ideas on biological pattern and the events that led to their wider acceptance by biologists as a valid way to investigate developmental pattern, and of the value of theory more generally in biology. Periodic patterns have played a key role in this process, especially 2D arrays of oriented stripes, which proved a disappointment in theoretical terms in the case of Drosophila segmentation, but a boost to theory as applied to skin patterns in fish and model chemical reactions. The concept of “order from fluctuations” is a key component of Turing’s theory, wherein pattern arises by selective amplification of spatial components concealed in the random disorder of molecular and/or cellular processes. For biological examples, a crucial point from an analytical standpoint is knowing the nature of the fluctuations, where the amplifier resides, and the timescale over which selective amplification occurs. The answer clarifies the difference between “inelegant” examples such as Drosophila segmentation, which is perhaps better understood as a programmatic assembly process, and “elegant” ones expressible in equations like Turing’s: that the fluctuations and selection process occur predominantly in evolutionary time for the former, but in real time for the latter, and likewise for error suppression, which for Drosophila is historical, in being lodged firmly in past evolutionary events. The prospects for a further extension of Turing’s ideas to the complexities of brain development and consciousness is discussed, where a case can be made that it could well be in neuroscience that his ideas find their most important application.

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Time and space in segmentation

Cited by 12 publications

References 281 publications

A timer gene network is spatially regulated by the terminal system in theDrosophilaembryo

A timer gene network is spatially regulated by the terminal system in theDrosophilaembryo

The organizing role of Wnt signaling pathway during arthropod posterior growth

Patterning, From Conifers to Consciousness: Turing’s Theory and Order From Fluctuations

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