Interplay between a Wnt-dependent organiser and the Notch segmentation clock regulates posterior development in <i>Periplaneta americana</i>

Chesebro, John; Pueyo, José Ignacio; Couso, Juan Pablo

doi:10.1242/bio.20123699

Cited by 56 publications

(69 citation statements)

References 67 publications

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“…In embryos of the cockroach Periplaneta, there is feedback between Wnt1 and Dl in the SAZ, and Wnt1 also activates cad to generate a signalling centre responsible for the generation of posterior segments (Chesebro et al, 2013). Unlike in Parasteatoda, however, cad represses Dl in the Periplaneta SAZ (Chesebro et al, 2013).…”

Section: Pt-eve and Pt-run-1 Do Not Regulate Each Othermentioning

confidence: 99%

“…In contrast to the regulation of segment formation in Drosophila and possibly other holometabolous insects, the formation of the SAZ and generation of posterior segments in many short-germ arthropods is regulated by a probably ancestral GRN that includes the Delta-Notch signalling pathway (Stollewerk et al, 2003;Schoppmeier and Damen, 2005a;Oda et al, 2007;Chipman and Akam, 2008;Pueyo et al, 2008), together with Wnt signalling (Bolognesi et al, 2008;McGregor et al, 2008b) and caudal (cad) Chesebro et al, 2013). Further understanding the underlying interactions in this GRN and how it directs segmentation in short-germ arthropods can provide much needed new insights into the evolution of these processes.…”

Section: Introductionmentioning

confidence: 99%

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The Wnt and Delta-Notch signalling pathways interact to direct pair-rule gene expression via caudal during segment addition in the spider Parasteatoda tepidariorum

et al. 2016

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In short-germ arthropods, posterior segments are added sequentially from a segment addition zone (SAZ) during embryogenesis. Studies in spiders such as Parasteatoda tepidariorum have provided insights into the gene regulatory network (GRN) underlying segment addition, and revealed that Wnt8 is required for dynamic Delta (Dl) expression associated with the formation of new segments. However, it remains unclear how these pathways interact during SAZ formation and segment addition. Here, we show that Delta-Notch signalling is required for Wnt8 expression in posterior SAZ cells, but represses the expression of this Wnt gene in anterior SAZ cells. We also found that these two signalling pathways are required for the expression of the spider orthologues of even-skipped (eve) and runt-1 (run-1), at least in part via caudal (cad). Moreover, it appears that dynamic expression of eve in this spider does not require a feedback loop with run-1, as is found in the pair-rule circuit of the beetle Tribolium. Taken together, our results suggest that the development of posterior segments in Parasteatoda is directed by dynamic interactions between Wnt8 and Delta-Notch signalling that are read out by cad, which is necessary but probably not sufficient to regulate the expression of eve and run-1. Our study therefore provides new insights towards better understanding the evolution and developmental regulation of segmentation in other arthropods, including insects.

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Section: Pt-eve and Pt-run-1 Do Not Regulate Each Othermentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The Wnt and Delta-Notch signalling pathways interact to direct pair-rule gene expression via caudal during segment addition in the spider Parasteatoda tepidariorum

et al. 2016

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“…Increasing molecular developmental data demonstrates evidence for a convergent origin of segmentation (see Shankland and Seaver, 2000;Seaver, 2003;De Rosa et al, 2005;Seaver et al, 2012). However, others have proposed that the last common ancestor of Bilateria was already segmented (de Robertis et al, 2008;Couso, 2009;Chesebro et al, 2013).…”

Section: Segmentationmentioning

confidence: 99%

Systematics, evolution and phylogeny of Annelida – a morphological perspective

Purschke¹,

Bleidorn²,

Struck³

2014

Mem. Mus. Vic.

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Purschke, G., Bleidorn, C. and Struck, T. 2014. Systematics, evolution and phylogeny of Annelida -a morphological perspective . Memoirs of Museum Victoria 71: 247-269.Annelida, traditionally divided into Polychaeta and Clitellata, is an evolutionary ancient and ecologically important group today usually considered to be monophyletic. However, there is a long debate regarding the in-group relationships as well as the direction of evolutionary changes within the group. This debate is correlated to the extraordinary evolutionary diversity of this group. Although annelids may generally be characterised as organisms with multiple repetitions of identically organised segments and usually bearing certain other characters such as a collagenous cuticle, chitinous chaetae or nuchal organs, none of these are present in every subgroup. This is even true for the annelid key character, segmentation. The first morphology-based cladistic analyses of polychaetes showed Polychaeta and Clitellata as sister groups. The former were divided into Scolecida and Palpata comprising Aciculata and Canalipalpata. This systematisation definitely replaced the old concept of dividing polychaetes into Errantia and Sedentaria, whereas the group Archiannelida had already been abandoned. The main critics came from a contradicting hypothesis relying on scenario based on plausibility considerations regarding Clitellata as highly derived annelids nesting within polychaetes and rendering the latter paraphyletic. In this hypothesis the absences of typical polychaete characters were regarded as losses rather than as primary absences. However, to date attempts to unambiguously identify the sister group of Clitellata on the basis of morphological characters have failed. Thus, two hypotheses on the last common annelid ancestor have been put forward either being an oligochaete-like burrowing animal or a parapodia-bearing epibenthic worm. These attempts to understand the major transitions in annelid evolution are reviewed and discussed in the light of new morphological evidence such as photoreceptor cell and eye evolution as well as the evolution of the nervous system and musculature. We also discuss the plausibility of these scenarios with regard to recent advances in molecular phylogenetic analyses.

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“…Typically if variation exists in segment period, it is simply a gradual decrease in segmentation rate as segmentation 'winds down' in the posterior of the embryo 6 or a brief initial period of rapid addition prior to a more regular rate 7 . A clock mechanism for regulating segmentation has recently been extended to sequentially segmenting arthropods [8][9][10][11][12][13] . Support for a clock includes a clear demonstration of molecular oscillations in the flour beetle, Trobolium casteneum 14 .…”

mentioning

confidence: 99%

Changing cell behaviours during beetle embryogenesis correlates with slowing of segmentation

Nakamoto

Hester²,

Constantinou

et al. 2015

Nat Commun

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Segmented animals are found in major clades as phylogenetically distant as vertebrates and arthropods. Typically, segments form sequentially in what has been thought to be a regular process, relying on a segmentation clock to pattern budding segments and posterior mitosis to generate axial elongation. Here we show that segmentation in Tribolium has phases of variable periodicity during which segments are added at different rates. Furthermore, elongation during a period of rapid posterior segment addition is driven by high rates of cell rearrangement, demonstrated by differential fates of marked anterior and posterior blastoderm cells. A computational model of this period successfully reproduces elongation through cell rearrangement in the absence of cell division. Unlike current models of steady-state sequential segmentation and elongation from a proliferative growth zone, our results indicate that cell behaviours are dynamic and variable, corresponding to differences in segmentation rate and giving rise to morphologically distinct regions of the embryo.

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Interplay between a Wnt-dependent organiser and the Notch segmentation clock regulates posterior development in Periplaneta americana

Cited by 56 publications

References 67 publications

The Wnt and Delta-Notch signalling pathways interact to direct pair-rule gene expression via caudal during segment addition in the spider Parasteatoda tepidariorum

The Wnt and Delta-Notch signalling pathways interact to direct pair-rule gene expression via caudal during segment addition in the spider Parasteatoda tepidariorum

Systematics, evolution and phylogeny of Annelida – a morphological perspective

Changing cell behaviours during beetle embryogenesis correlates with slowing of segmentation

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