Neuronal development in larval polychaete <i>Phyllodoce maculata</i> (Phyllodocidae)

Voronezhskaya, Elena E.; Tsitrin, E. B.; Nezlin, Leonid P.

doi:10.1002/cne.10488

Cited by 90 publications

(122 citation statements)

References 44 publications

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“…Furthermore, the serotonergic and FMRFamidergic immunoreactivity in P. massiliensis only originates in anterior regions. For P. dumerilii and most other annelid larvae, the origin of FMRFamidergic immunoreactivity is described to appear at the anterior pole, whereas serotonin immunoreactivity can be found first at the posterior pole (Voronezhskaya et al, 2003;Orrhage and Müller, 2005;Wanninger et al, 2005;McDougall et al, 2006;Brinkmann and Wanninger, 2008;Kristof et al, 2008;Fischer et al, 2010;Helm et al, 2013;). Similarly, the serotonergic immunoreactivity is detectable first…”

Section: Discussionmentioning

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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Section: Discussionmentioning

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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“…A pair of ''pioneer'' nerve cells at the pygidium with axons extending forwards to the prototroch has been observed in 48-hours metatrochophores of Platynereis (Dorresteijn et al,'93) and a single such cell has been observed in an early stage of Phyllodoce (Voronezhskaya et al, 2003), and also in early larvae of Serpula oregonensis (by Dr. Stephen Kempf and the author). The significance of these cells is unknown.…”

Section: Apical Organ and Adult Brainmentioning

confidence: 98%

Trochophora larvae: Cell‐lineages, ciliary bands, and body regions. 1. Annelida and Mollusca

2004

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The trochophora concept and the literature on cleavage patterns and differentiation of ectodermal structures in annelids (''polychaetes'') and molluscs are reviewed. The early development shows some variation within both phyla, and the cephalopods have a highly modified development. Nevertheless, there are conspicuous similarities between the early development of the two phyla, related to the highly conserved spiral cleavage pattern. Apical and cerebral ganglia have almost identical origin in the two phyla, and the cell-lineage of the prototroch is identical, except for minor variations between species. The cell-lineage of the metatrochs is almost unknown, but the telotroch of annelids and the ''telotroch'' of the gastropod Patella originate from the 2d-cell, as does the gastrotroch in the few species which have been studied. The segmented annelid body, i.e. the region behind the peristome, develops through addition of new ectoderm from a ring of 2d-cells just in front of the telotroch. This whole region is thus derived from 2d-cells. Conversely, the mollusc body is covered by descendants of cells from both the C and D quadrants and a growth zone is not apparent. This supports the notion that the molluscs are not segmented like the annelids, and that the repeated structures seen in polyplacophorans and monplacophorans do not represent a segmentation homologous to that of the annelids.

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“…Anatomical studies have revealed that larval ciliary bands receive extensive innervation from the nervous system, both in Platynereis and in other species (21). In protostome larvae, neurons expressing the neuropeptide FMRF-amide often contribute to this innervation (22)(23)(24). Neurons with related Famide neuropeptides also innervate ciliary bands in sea urchin larvae (25), suggesting that neuropeptides may have a general role in the regulation of larval locomotion in both protostomes and deuterostomes.…”

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confidence: 99%

Neuropeptides regulate swimming depth of Platynereis larvae

Conzelmann

Offenburger

Asadulina

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

118

180

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Cilia-based locomotion is the major form of locomotion for microscopic planktonic organisms in the ocean. Given their negative buoyancy, these organisms must control ciliary activity to maintain an appropriate depth. The neuronal bases of depth regulation in ciliary swimmers are unknown. To gain insights into depth regulation we studied ciliary locomotor control in the planktonic larva of the marine annelid, Platynereis. We found several neuropeptides expressed in distinct sensory neurons that innervate locomotor cilia. Neuropeptides altered ciliary beat frequency and the rate of calcium-evoked ciliary arrests. These changes influenced larval orientation, vertical swimming, and sinking, resulting in upward or downward shifts in the steady-state vertical distribution of larvae. Our findings indicate that Platynereis larvae have depth-regulating peptidergic neurons that directly translate sensory inputs into locomotor output on effector cilia. We propose that the simple circuitry found in these ciliated larvae represents an ancestral state in nervous system evolution.neural circuit | zooplankton | sensory-motor neuron | FMRFamide-related peptides T wo different types of locomotor systems are present in animals, one muscle based and the other cilia based. The neuronal control of muscle-based motor systems is well understood from studies on terrestrial model organisms. In contrast, our knowledge of the neuronal control of ciliary locomotion is limited, even though cilia-driven locomotion is prominent in the majority of animal phyla (1).Ciliary swimming in open water is widespread among the larval stages of marine invertebrates, including sponges, cnidarians, and many protostomes and deuterostomes (2-5). Freely swimming ciliated larvae often spend days to months as part of the zooplankton (1, 6). The primary axis for ciliated plankton is vertical, and body orientation is maintained either by passive (buoyancy) or active (gravitaxis, phototaxis) mechanisms. When cilia beat, larvae swim upward, and when cilia cease beating, the negatively buoyant larvae sink. During swimming, the thrust exerted on the body is proportional to the beating frequency of cilia (7-9). The alternation of active upward swimming and passive sinking, together with swimming speed and sinking rate, is thought to determine vertical distribution in the water (8). Because several environmental parameters, including water temperature, light intensity, and phytoplankton abundance, change with depth, swimming depth will influence the speed of larval development, the magnitude of UV damage, and the success of larval feeding and settlement. To stay at an appropriate depth, planktonic swimmers must therefore sense environmental cues and regulate ciliary beating.The ciliated larvae of the marine annelid Platynereis dumerilii provide an accessible model for the study of ciliary swimming in marine plankton (10). Platynereis can be cultured in the laboratory, and thousands of synchronously developing larvae can be obtained daily year-round (11). Platynereis ha...

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Neuronal development in larval polychaete Phyllodoce maculata (Phyllodocidae)

Cited by 90 publications

References 44 publications

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

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

Trochophora larvae: Cell‐lineages, ciliary bands, and body regions. 1. Annelida and Mollusca

Neuropeptides regulate swimming depth of Platynereis larvae

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