Hedgehog Signaling Regulates Segment Formation in the Annelid
            <i>Platynereis</i>

Dray, Nicolas; Tessmar-Raible, Kristin; Gouar, Martine Le; Vibert, Laura; Christodoulou, Foteini; Schipany, Katharina; Guillou, Aurélien; Zantke, Juliane; Snyman, Heidi; Béhague, Julien; Vervoort, Michel; Arendt, Detlev; Balavoine, Guillaume

doi:10.1126/science.1188913

Cited by 88 publications

(81 citation statements)

References 21 publications

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“…-So far, relatively few similarities have been found at the genetic level between segment formation processes in distant phyla, with two important exceptions: the existence of analogous "segmentation clocks" in short germ insects and vertebrates (Sarrazin et al, 2012) and the similar roles of Hedgehog signalling in segment polarity in arthropods and annelids (Dray et al, 2010). It can be argued that this relative paucity of evidence is partly a consequence of our ignorance.…”

Section: Introductionmentioning

confidence: 96%

Segment formation in Annelids: patterns, processes and evolution

Balavoine¹

2014

Int. J. Dev. Biol.

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The debate on the origin of segmentation is a central question in the study of body plan evolution in metazoans. Annelids are the most conspicuously metameric animals as most of the trunk is formed of identical anatomical units. In this paper, I summarize the various patterns of evolution of the metameric body plan in annelids, showing the remarkable evolvability of this trait, similar to what is also found in arthropods. I then review the different modes of segment formation in the annelid tree, taking into account the various processes taking place in the life histories of these animals, including embryogenesis, post-embryonic development, regeneration and asexual reproduction. As an example of the variations that occur at the cellular and genetic level in annelid segment formation, I discuss the processes of teloblastic growth or posterior addition in key groups in the annelid tree. I propose a comprehensive definition for the teloblasts, stem cells that are responsible for sequential segment addition. There are a diversity of different mechanisms used in annelids to produce segments depending on the species, the developmental time and also the life history processes of the worm. A major goal for the future will be to reconstitute an ancestral process (or several ancestral processes) in the ancestor of the whole clade. This in turn will provide key insights in the current debate on ancestral bilaterian segmentation.

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Section: Introductionmentioning

confidence: 96%

Segment formation in Annelids: patterns, processes and evolution

Balavoine¹

2014

Int. J. Dev. Biol.

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“…the nervous system in Bilateria (Prud'homme et al, 2003;Arendt et al, 2004;Denes et al, 2007;Tessmar-Raible et al, 2007;Jekely et al, 2008;Dray et al, 2010;Tomer et al, 2010).…”

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confidence: 99%

“…Biol. 58: 613-622 (2014) doi: 10.1387/ijdb.140081cb the nervous system in Bilateria (Prud'homme et al, 2003;Arendt et al, 2004; Denes et al, 2007;Tessmar-Raible et al, 2007;Jekely et al, 2008;Dray et al, 2010;Tomer et al, 2010).Platynereis dumerilii is a marine annelid of the family Nereididae, which are part of the Errantia (Struck et al, 2011; Weigert et al, in press). The life cycle is well established and controlled in the lab and this gonochoric species has an indirect development, with planktotrophic larvae (Fischer and Dorresteijn, 2004).…”

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confidence: 99%

An immunocytochemical window into the development of Platynereis massiliensis (Annelida, Nereididae)

Helm¹,

Adamo²,

Hourdez³

et al. 2014

Int. J. Dev. Biol.

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The nereidid annelid Platynereis dumerilii emerged as a well-understood model organism. P. dumerilii and P. massiliensis are sister taxa, which are morphologically indistinguishable as adults. Interestingly, they exhibit highly contrasting life-histories: while P. dumerilii is a gonochorostic species with planktonic feeding larvae, P. massiliensis is a protandric hermaphrodite with lecitotrophic semi-direct -development in brood tubes. Using light microscopy and immunohistochemical methods coupled with confocal laser scanning microscopy, we describe the development of P. massiliensis. Musculature was stained with phalloidin-rhodamine. FMRFamide, acetylated a-tubulin, and serotonin were targeted by antibodies for the staining of neuronal structures. Additionally, eye development was investigated with the specific 22C10-antibody. The development of P. massiliensis is characterized by the absence of a free-swimming stage, a late development of food uptake, and the presence of a large amount of yolk even in late juvenile stages. Most notably, early juvenile stages already exhibit an organization of several organ systems that resembles those of adults. Larval characters present in the free-swimming feeding larvae of P. dumerilii, as e.g. the apical organ and larval eyes, are absent and regarded to be lost in developing stages of P. massiliensis. Many of the differences found in the development of these two species can be described in the context of heterochronic changes. We strongly advocate expanding evolutionary developmental studies from the well-established model annelid P. dumerilii to the closely related P. massiliensis to study the evolutionary conservation and divergence of genetic pathways involved in developmental processes. KEY WORDS: cLSM, evodevo, eye development, heterochrony, model organism, polychaeteThe vast majority of bilaterian animals are classified into three large clades: Deuterostomia, Ecdysozoa and Lophotrochozoa. Whereas several animal model systems for evolutionary developmental research are well established for the former two taxa, lophotrochozoans are underrepresented in this regard (GIGA Community of Scientists, 2014). However, especially in the last decade the annelid Platynereis dumerilii emerged as a well-understood model species (Fischer and Dorresteijn, 2004;Fischer et al., 2010;Simakov et al., 2013). Consequently, techniques as whole mount in situ hybridization, cell ablation, RNAinterference, and morpholino knockdowns are well established (Tessmar-Raible and Arendt, 2003;Veedin-Rajan et al., 2013). Moreover, transgenic lineages have been created (Backfisch et al., 2013) and a genome sequencing project is underway for this species (http://4dx.embl.de/platy/). Evolutionary developmental studies on Platynereis dumerilii provided important insights into the evolution of segmentation, vision and Int. J. Dev. Biol. 58: 613-622 (2014) doi: 10.1387/ijdb.140081cb the nervous system in Bilateria (Prud'homme et al., 2003;Arendt et al., 2004; Denes et al., 2007;Tessmar-Raible et al...

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“…L'expression des composants des voies de signalisation a suggéré que l'on pouvait retrouver chez l'ancêtre métazoaire des rôles similaires à ceux des bilaté-riens. Chez Amphimedon, l'expression du ligand Hedgling (apparenté à Hedgehog) délimite l'anneau pigmentaire lorsqu'il se développe, ce qui rappelle le rôle de cette voie dans la démarcation de segments chez la drosophile et l'annélide Platynereis [10,14]. La voie Notch, elle, comme chez les bilatériens, semble être utilisée pour donner différentes identités à deux cellules filles pendant la division cellulaire [15].…”

Section: Le Développement Des Premiers Animauxunclassified

Le génome de l’épongeAmphimedon queenslandicanous aide à reconstruire notre ancêtre précambrien

Larroux¹

2011

Med Sci (Paris)

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Hedgehog Signaling Regulates Segment Formation in the Annelid Platynereis

Cited by 88 publications

References 21 publications

Segment formation in Annelids: patterns, processes and evolution

Segment formation in Annelids: patterns, processes and evolution

An immunocytochemical window into the development of Platynereis massiliensis (Annelida, Nereididae)

Le génome de l’épongeAmphimedon queenslandicanous aide à reconstruire notre ancêtre précambrien

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