Photoreceptor cells and eyes in Annelida

Purschke, Günter; Arendt, Detlev; Hausen, Harald; Müller, Mónika

doi:10.1016/j.asd.2006.07.005

Cited by 91 publications

(148 citation statements)

References 75 publications

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“…A single unmodified cilium (Fig. 3 D and E), which is often found in microvillar PRCs (20,21), does not appear to contribute extensively to surface enlargement and, hence, we can clearly classify the SpOpsin4-expressing cells as a microvillar PRC type. The PRC cytoplasm makes the cells easily distinguishable from all surrounding nerve cell types by being completely filled with numerous clear vesicles of differing size (Fig.…”

Section: Resultsmentioning

confidence: 99%

Unique system of photoreceptors in sea urchin tube feet

Ullrich-Lüter

Dupont

Arboleda

et al. 2011

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

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Different sea urchin species show a vast variety of responses to variations in light intensity; however, despite this behavioral evidence for photosensitivity, light sensing in these animals has remained an enigma. Genome information of the recently sequenced purple sea urchin (Strongylocentrotus purpuratus) allowed us to address this question from a previously unexplored molecular perspective by localizing expression of the rhabdomeric opsin Spopsin4 and Sp-pax6, two genes essential for photoreceptor function and development, respectively. Using a specifically designed antibody against Sp-Opsin4 and in situ hybridization for both genes, we detected expression in two distinct groups of photoreceptor cells (PRCs) located in the animal's numerous tube feet. Specific reactivity of the Sp-Opsin4 antibody with sea star optic cushions, which regulate phototaxis, suggests a similar visual function in sea urchins. Ultrastructural characterization of the sea urchin PRCs revealed them to be of a microvillar receptor type. Our data suggest that echinoderms, in contrast to chordates, deploy a microvillar, r-opsinexpressing PRC type for vision, a feature that has been so far documented only in protostome animals. Surprisingly, sea urchin PRCs lack any associated screening pigment. Indeed, one of the tube foot PRC clusters may account for directional vision by being shaded through the opaque calcite skeleton. The PRC axons connect to the animal internal nervous system, suggesting an integrative function beyond local short circuits. Because juveniles display no phototaxis until skeleton completion, we suggest a model in which the entire sea urchin, deploying its skeleton as PRC screening device, functions as a huge compound eye.evolution | electron microscopy | immunogold

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Section: Resultsmentioning

confidence: 99%

Unique system of photoreceptors in sea urchin tube feet

Ullrich-Lüter

Dupont

Arboleda

et al. 2011

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

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132

160

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“…These conditions resemble the morphology of P. dumerilii shortly before metamorphosis (Fischer et al, 2010, Steinmetz et al, 2011. In annelids, larvae usually exhibit a pair of single eyes consisting of one pigment cell and one photoreceptor cell, whereas most adults of Phyllodocida and Eunicida (including Nereididae) possess two pairs of so-called cerebral eyes (Purschke, 2005;Purschke et al, 2006). The ontogenetic studies on the presence of pigment cells and the staining with the 22C10 antibody support the pres- ence of two adult-like eyes even in early juveniles of P. massiliensis.…”

Section: B C D E F Amentioning

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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“…This transition appears to be paralleled by the change from using ciliary bands in locomotion such as those present in planktotrophic metazoan larvae to muscular systems. In such systems, integrative neuronal processes coordinate the activity of several longitudinal and circular or transverse muscle fibres (see, for example, Tzetlin & Filippova 2005;Purschke & Müller 2006). This larva-to-adult transition involves the development of two different sets of eyes in many invertebrates: larval eyes directly associated with the ciliated cells such as those recently described by Jékely et al (2008) and adult eyes with neuronal projections into the central nervous system (as is present, for example, in Platynereis; see Jékely et al 2008 and references therein).…”

Section: The Evolution Of Visual Eyes and Bipolar Interneuronsmentioning

confidence: 99%

The ‘division of labour’ model of eye evolution

Arendt

Hausen

Purschke

2009

Phil. Trans. R. Soc. B

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The 'division of labour' model of eye evolution is elaborated here. We propose that the evolution of complex, multicellular animal eyes started from a single, multi-functional cell type that existed in metazoan ancestors. This ancient cell type had at least three functions: light detection via a photoreceptive organelle, light shading by means of pigment granules and steering through locomotor cilia. Located around the circumference of swimming ciliated zooplankton larvae, these ancient cells were able to mediate phototaxis in the absence of a nervous system. This precursor then diversified, by cell-type functional segregation, into sister cell types that specialized in different subfunctions, evolving into separate photoreceptor cells, shading pigment cells (SPCs) or ciliated locomotor cells. Photoreceptor sensory cells and ciliated locomotor cells remained interconnected by newly evolving axons, giving rise to an early axonal circuit. In some evolutionary lines, residual functions prevailed in the specialized cell types that mirror the ancient multi-functionality, for instance, SPCs expressing an opsin as well as possessing rhabdomer-like microvilli, vestigial cilia and an axon. Functional segregation of cell types in eye evolution also explains the emergence of more elaborate photosensory-motor axonal circuits, with interneurons relaying the visual information.

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Photoreceptor cells and eyes in Annelida

Cited by 91 publications

References 75 publications

Unique system of photoreceptors in sea urchin tube feet

Unique system of photoreceptors in sea urchin tube feet

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

The ‘division of labour’ model of eye evolution

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