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Molecular characterization of the apical organ of the anthozoan Nematostella vectensis.

Sinigaglia C, Busengdal H, Lerner A, Oliveri P, Rentzsch F - Dev. Biol. (2014)

Bottom Line: In bilaterians they are characterised by a tuft of long cilia and receptor cells and they are associated with groups of neurons, but their relatively low morphological complexity and dispersed phylogenetic distribution have left their evolutionary relationship unresolved.To provide a foundation for a better understanding of this structure we have characterised the molecular composition of the apical organ of the sea anemone Nematostella vectensis.Our study provides a molecular characterization of the apical organ of Nematostella and represents an informative tool for future studies addressing the development, function and evolutionary history of apical organ cells.

View Article: PubMed Central - PubMed

Affiliation: Sars Centre for Marine Molecular Biology, University of Bergen, Thormøhlensgt 55, 5008 Bergen, Norway.

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Nematostella vectensis as a model for the identification of apical organ genes (A) Apical organs are found in the developing stages of diverse invertebrates: Cnidaria, Lophotrochozoa, Echinodermata and Hemichordata (red asterisks). (B) N. vectensis is a representative of the Anthozoa, the sister group to all other cnidarians. Anthozoa is the only class of Cnidaria where apical organs with long cilia have been described. Embryonic development comprehends a swimming stage, the planula larva, which bears a tuft of long cilia at the aboral pole. The apical organ disappears after about one week of development, when the larva settles and develops the tentacles. (C) Experimental design for the microarray analysis. Apical organs (red tuft in the drawing) were manipulated by injecting antisense morpholinos directed against two FGF ligands with opposite functions: NvFGFa1 MO produces larvae lacking an apical organ, while NvFGFa2 MO leads to larvae with an expanded organ. The samples were preserved until total RNA was extracted from the different conditions (including the control wild type). The transcription profiles of the three phenotypes were compared in a microarray analysis.
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f0005: Nematostella vectensis as a model for the identification of apical organ genes (A) Apical organs are found in the developing stages of diverse invertebrates: Cnidaria, Lophotrochozoa, Echinodermata and Hemichordata (red asterisks). (B) N. vectensis is a representative of the Anthozoa, the sister group to all other cnidarians. Anthozoa is the only class of Cnidaria where apical organs with long cilia have been described. Embryonic development comprehends a swimming stage, the planula larva, which bears a tuft of long cilia at the aboral pole. The apical organ disappears after about one week of development, when the larva settles and develops the tentacles. (C) Experimental design for the microarray analysis. Apical organs (red tuft in the drawing) were manipulated by injecting antisense morpholinos directed against two FGF ligands with opposite functions: NvFGFa1 MO produces larvae lacking an apical organ, while NvFGFa2 MO leads to larvae with an expanded organ. The samples were preserved until total RNA was extracted from the different conditions (including the control wild type). The transcription profiles of the three phenotypes were compared in a microarray analysis.

Mentions: Apical organs are found in the larval stages of phylogenetically diverse animal groups (Fig. 1A) such as anthozoan cnidarians, protostomes (e.g. molluscs and annelids) and deuterostomes (e.g. echinoderms and hemichordates). The functions of apical organs are not well understood and may vary between taxa. Given their temporal restriction to larval stages, apical organs have been proposed to play an important role in the detection of settlement cues and for the induction of metamorphosis, presumably acting as chemosensory and/or mechanosensory structures. Such a function has been confirmed by functional approaches in only few species (Conzelmann et al., 2013; Hadfield et al., 2000; Kempf et al., 1997; Rentzsch et al., 2008; Voronezhskaya and Khabarova, 2003; Voronezhskaya et al., 2004). The regulation of this life cycle transition not only represents a key developmental, but also an important ecological role, since the recruitment to the substrate and the metamorphosis of swimming larvae contribute to the shaping of benthic communities (e.g. Shikuma et al., 2014; Siboni et al., 2014; Witt et al., 2011). Moreover, apical organs are thought to regulate the activity of ciliary bands and musculature in some bilaterians and thus likely contribute to their locomotion (Croll and Dickinson, 2004; Goldberg et al., 1994; Satterlie and Cameron, 1985).


Molecular characterization of the apical organ of the anthozoan Nematostella vectensis.

Sinigaglia C, Busengdal H, Lerner A, Oliveri P, Rentzsch F - Dev. Biol. (2014)

Nematostella vectensis as a model for the identification of apical organ genes (A) Apical organs are found in the developing stages of diverse invertebrates: Cnidaria, Lophotrochozoa, Echinodermata and Hemichordata (red asterisks). (B) N. vectensis is a representative of the Anthozoa, the sister group to all other cnidarians. Anthozoa is the only class of Cnidaria where apical organs with long cilia have been described. Embryonic development comprehends a swimming stage, the planula larva, which bears a tuft of long cilia at the aboral pole. The apical organ disappears after about one week of development, when the larva settles and develops the tentacles. (C) Experimental design for the microarray analysis. Apical organs (red tuft in the drawing) were manipulated by injecting antisense morpholinos directed against two FGF ligands with opposite functions: NvFGFa1 MO produces larvae lacking an apical organ, while NvFGFa2 MO leads to larvae with an expanded organ. The samples were preserved until total RNA was extracted from the different conditions (including the control wild type). The transcription profiles of the three phenotypes were compared in a microarray analysis.
© Copyright Policy - CC BY
Related In: Results  -  Collection

License
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getmorefigures.php?uid=PMC4300403&req=5

f0005: Nematostella vectensis as a model for the identification of apical organ genes (A) Apical organs are found in the developing stages of diverse invertebrates: Cnidaria, Lophotrochozoa, Echinodermata and Hemichordata (red asterisks). (B) N. vectensis is a representative of the Anthozoa, the sister group to all other cnidarians. Anthozoa is the only class of Cnidaria where apical organs with long cilia have been described. Embryonic development comprehends a swimming stage, the planula larva, which bears a tuft of long cilia at the aboral pole. The apical organ disappears after about one week of development, when the larva settles and develops the tentacles. (C) Experimental design for the microarray analysis. Apical organs (red tuft in the drawing) were manipulated by injecting antisense morpholinos directed against two FGF ligands with opposite functions: NvFGFa1 MO produces larvae lacking an apical organ, while NvFGFa2 MO leads to larvae with an expanded organ. The samples were preserved until total RNA was extracted from the different conditions (including the control wild type). The transcription profiles of the three phenotypes were compared in a microarray analysis.
Mentions: Apical organs are found in the larval stages of phylogenetically diverse animal groups (Fig. 1A) such as anthozoan cnidarians, protostomes (e.g. molluscs and annelids) and deuterostomes (e.g. echinoderms and hemichordates). The functions of apical organs are not well understood and may vary between taxa. Given their temporal restriction to larval stages, apical organs have been proposed to play an important role in the detection of settlement cues and for the induction of metamorphosis, presumably acting as chemosensory and/or mechanosensory structures. Such a function has been confirmed by functional approaches in only few species (Conzelmann et al., 2013; Hadfield et al., 2000; Kempf et al., 1997; Rentzsch et al., 2008; Voronezhskaya and Khabarova, 2003; Voronezhskaya et al., 2004). The regulation of this life cycle transition not only represents a key developmental, but also an important ecological role, since the recruitment to the substrate and the metamorphosis of swimming larvae contribute to the shaping of benthic communities (e.g. Shikuma et al., 2014; Siboni et al., 2014; Witt et al., 2011). Moreover, apical organs are thought to regulate the activity of ciliary bands and musculature in some bilaterians and thus likely contribute to their locomotion (Croll and Dickinson, 2004; Goldberg et al., 1994; Satterlie and Cameron, 1985).

Bottom Line: In bilaterians they are characterised by a tuft of long cilia and receptor cells and they are associated with groups of neurons, but their relatively low morphological complexity and dispersed phylogenetic distribution have left their evolutionary relationship unresolved.To provide a foundation for a better understanding of this structure we have characterised the molecular composition of the apical organ of the sea anemone Nematostella vectensis.Our study provides a molecular characterization of the apical organ of Nematostella and represents an informative tool for future studies addressing the development, function and evolutionary history of apical organ cells.

View Article: PubMed Central - PubMed

Affiliation: Sars Centre for Marine Molecular Biology, University of Bergen, Thormøhlensgt 55, 5008 Bergen, Norway.

Show MeSH