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Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords.

Kaul-Strehlow S, Urata M, Minokawa T, Stach T, Wanninger A - Org. Divers. Evol. (2015)

Bottom Line: We found that all serotonin-like immunoreactive (LIR) neurons in both species are bipolar ciliary neurons that are intercalated between other epidermal cells.Unlike the tornaria larva of B. misakiensis, the embryonic nervous system of S. kowalevskii lacks serotonin-LIR neurons in the apical region as well as an opisthotroch neurite ring.Our data reveal a highly conserved mode of neurogenesis in enteropneusts that is independent of the developing mode and is inferred to be a common feature for Enteropneusta.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Zoology, University of Vienna, Althanstr. 14, 1090 Vienna, Austria.

ABSTRACT

Concerning the evolution of deuterostomes, enteropneusts (acorn worms) occupy a pivotal role as they share some characteristics with chordates (e.g., tunicates and vertebrates) but are also closely related to echinoderms (e.g., sea urchin). The nervous system in particular can be a highly informative organ system for evolutionary inferences, and advances in fluorescent microscopy have revealed overwhelming data sets on neurogenesis in various clades. However, immunocytochemical descriptions of neurogenesis of juvenile enteropneusts are particularly scarce, impeding the reconstruction of nervous system evolution in this group. We followed morphogenesis of the nervous system in two enteropneust species, one with direct (Saccoglossus kowalevskii) and the other with indirect development (Balanoglossus misakiensis), using an antibody against serotonin and electron microscopy. We found that all serotonin-like immunoreactive (LIR) neurons in both species are bipolar ciliary neurons that are intercalated between other epidermal cells. Unlike the tornaria larva of B. misakiensis, the embryonic nervous system of S. kowalevskii lacks serotonin-LIR neurons in the apical region as well as an opisthotroch neurite ring. Comparative analysis of both species shows that the projections of the serotonin-LIR somata initially form a basiepidermal plexus throughout the body that disappears within the trunk region soon after settlement before the concentrated dorsal and ventral neurite bundles emerge. Our data reveal a highly conserved mode of neurogenesis in enteropneusts that is independent of the developing mode and is inferred to be a common feature for Enteropneusta. Moreover, all detected serotonin-LIR neurons are presumably receptor cells, and the absence of serotonin-LIR interneurons from the enteropneust nervous system, which are otherwise common in various bilaterian central nervous systems, is interpreted as a loss that might have occurred already in the last common ancestor of Ambulacraria.

No MeSH data available.


Related in: MedlinePlus

Neurogenesis in the 2-gill slit juvenile of B. misakiensis. a, b Scanning electron micrographs: c–i Z-projections of confocal microscopy image stacks. Anterior is to the right. a Dorsolateral view of a 3-day-old settled juvenile. b Higher magnification of the two gill slits and the dorsal tongue bars. c Overview of the 5-HT+ NS of a 3-day-old juvenile. d The collar cord is composed of three 5-HT+ neurite bundles of which the median one projects posteriorly into the dorsal nerve cord. e Detail of the ventral 5-HT+ neurite bundle with numerous incoming circular neurites emerging from lateral bipolar neurons. f Detail of the anterior part of the dorsal 5-HT+ neurite bundle and epidermal collar region. This part is discontinuous with the posterior part of the 5-HT neurite bundle shown in g, see also double arrowheads and dashed area. g The posterior part of the dorsal 5-HT+ neurite bundle contains few serotonin-LIR neurites and is discontinuous with the anterior part of the 5-HT neurite bundle, see double arrowheads and dashed area. h Partial Z- projection of a sagittal scan of the dorsal collar region. The collar cord comprises ventral neurite bundles and a dorsal sheath of somata, which are not serotonin-LIR positive. i Close-up of a part of the proboscis region showing the 5-HT+ bipolar neurons and the basiepidermal nervous plexus. 5-HT, serotonin; a, anus; ac-α-tub, acetylated α-tubulin; cn, circumferential neurite; cc, collar cord; ci, cilia; co, collar; dnb, dorsal neurite bundle; ep, epidermis; gs, gill slit; msp, mesocoel pore; nn, nervous plexus; onr, opisthotroch nerve ring; pnr, prebranchial nerve ring; pr, proboscis; ps, proboscis stem; sn, serotonin-LIR neuron; tb, tongue bar; tm, trunk musculature; vnb, ventral neurite bundle
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Fig5: Neurogenesis in the 2-gill slit juvenile of B. misakiensis. a, b Scanning electron micrographs: c–i Z-projections of confocal microscopy image stacks. Anterior is to the right. a Dorsolateral view of a 3-day-old settled juvenile. b Higher magnification of the two gill slits and the dorsal tongue bars. c Overview of the 5-HT+ NS of a 3-day-old juvenile. d The collar cord is composed of three 5-HT+ neurite bundles of which the median one projects posteriorly into the dorsal nerve cord. e Detail of the ventral 5-HT+ neurite bundle with numerous incoming circular neurites emerging from lateral bipolar neurons. f Detail of the anterior part of the dorsal 5-HT+ neurite bundle and epidermal collar region. This part is discontinuous with the posterior part of the 5-HT neurite bundle shown in g, see also double arrowheads and dashed area. g The posterior part of the dorsal 5-HT+ neurite bundle contains few serotonin-LIR neurites and is discontinuous with the anterior part of the 5-HT neurite bundle, see double arrowheads and dashed area. h Partial Z- projection of a sagittal scan of the dorsal collar region. The collar cord comprises ventral neurite bundles and a dorsal sheath of somata, which are not serotonin-LIR positive. i Close-up of a part of the proboscis region showing the 5-HT+ bipolar neurons and the basiepidermal nervous plexus. 5-HT, serotonin; a, anus; ac-α-tub, acetylated α-tubulin; cn, circumferential neurite; cc, collar cord; ci, cilia; co, collar; dnb, dorsal neurite bundle; ep, epidermis; gs, gill slit; msp, mesocoel pore; nn, nervous plexus; onr, opisthotroch nerve ring; pnr, prebranchial nerve ring; pr, proboscis; ps, proboscis stem; sn, serotonin-LIR neuron; tb, tongue bar; tm, trunk musculature; vnb, ventral neurite bundle

Mentions: After about 3-day postsettlement, most of the juveniles exhibit two pairs of gill slits (Fig. 5a, b). Both gill slits are U-shaped and heavily ciliated on the inside (Fig. 5b). No synapticles are developed. The juveniles measure up to 1.5 mm in total length (Fig. 5a–c). The proboscis shows the typical acorn shape, while the mesosome has developed into a 200-μm-long three-lobed collar region (Fig. 5a). Scanning electron micrographs and acetylated-α-tubulin-LIR reveal that the proboscis and collar region are evenly covered with cilia, whereas on the trunk region, only scattered tufts of cilia are present (Fig. 5a, c).Fig. 5


Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords.

Kaul-Strehlow S, Urata M, Minokawa T, Stach T, Wanninger A - Org. Divers. Evol. (2015)

Neurogenesis in the 2-gill slit juvenile of B. misakiensis. a, b Scanning electron micrographs: c–i Z-projections of confocal microscopy image stacks. Anterior is to the right. a Dorsolateral view of a 3-day-old settled juvenile. b Higher magnification of the two gill slits and the dorsal tongue bars. c Overview of the 5-HT+ NS of a 3-day-old juvenile. d The collar cord is composed of three 5-HT+ neurite bundles of which the median one projects posteriorly into the dorsal nerve cord. e Detail of the ventral 5-HT+ neurite bundle with numerous incoming circular neurites emerging from lateral bipolar neurons. f Detail of the anterior part of the dorsal 5-HT+ neurite bundle and epidermal collar region. This part is discontinuous with the posterior part of the 5-HT neurite bundle shown in g, see also double arrowheads and dashed area. g The posterior part of the dorsal 5-HT+ neurite bundle contains few serotonin-LIR neurites and is discontinuous with the anterior part of the 5-HT neurite bundle, see double arrowheads and dashed area. h Partial Z- projection of a sagittal scan of the dorsal collar region. The collar cord comprises ventral neurite bundles and a dorsal sheath of somata, which are not serotonin-LIR positive. i Close-up of a part of the proboscis region showing the 5-HT+ bipolar neurons and the basiepidermal nervous plexus. 5-HT, serotonin; a, anus; ac-α-tub, acetylated α-tubulin; cn, circumferential neurite; cc, collar cord; ci, cilia; co, collar; dnb, dorsal neurite bundle; ep, epidermis; gs, gill slit; msp, mesocoel pore; nn, nervous plexus; onr, opisthotroch nerve ring; pnr, prebranchial nerve ring; pr, proboscis; ps, proboscis stem; sn, serotonin-LIR neuron; tb, tongue bar; tm, trunk musculature; vnb, ventral neurite bundle
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4514687&req=5

Fig5: Neurogenesis in the 2-gill slit juvenile of B. misakiensis. a, b Scanning electron micrographs: c–i Z-projections of confocal microscopy image stacks. Anterior is to the right. a Dorsolateral view of a 3-day-old settled juvenile. b Higher magnification of the two gill slits and the dorsal tongue bars. c Overview of the 5-HT+ NS of a 3-day-old juvenile. d The collar cord is composed of three 5-HT+ neurite bundles of which the median one projects posteriorly into the dorsal nerve cord. e Detail of the ventral 5-HT+ neurite bundle with numerous incoming circular neurites emerging from lateral bipolar neurons. f Detail of the anterior part of the dorsal 5-HT+ neurite bundle and epidermal collar region. This part is discontinuous with the posterior part of the 5-HT neurite bundle shown in g, see also double arrowheads and dashed area. g The posterior part of the dorsal 5-HT+ neurite bundle contains few serotonin-LIR neurites and is discontinuous with the anterior part of the 5-HT neurite bundle, see double arrowheads and dashed area. h Partial Z- projection of a sagittal scan of the dorsal collar region. The collar cord comprises ventral neurite bundles and a dorsal sheath of somata, which are not serotonin-LIR positive. i Close-up of a part of the proboscis region showing the 5-HT+ bipolar neurons and the basiepidermal nervous plexus. 5-HT, serotonin; a, anus; ac-α-tub, acetylated α-tubulin; cn, circumferential neurite; cc, collar cord; ci, cilia; co, collar; dnb, dorsal neurite bundle; ep, epidermis; gs, gill slit; msp, mesocoel pore; nn, nervous plexus; onr, opisthotroch nerve ring; pnr, prebranchial nerve ring; pr, proboscis; ps, proboscis stem; sn, serotonin-LIR neuron; tb, tongue bar; tm, trunk musculature; vnb, ventral neurite bundle
Mentions: After about 3-day postsettlement, most of the juveniles exhibit two pairs of gill slits (Fig. 5a, b). Both gill slits are U-shaped and heavily ciliated on the inside (Fig. 5b). No synapticles are developed. The juveniles measure up to 1.5 mm in total length (Fig. 5a–c). The proboscis shows the typical acorn shape, while the mesosome has developed into a 200-μm-long three-lobed collar region (Fig. 5a). Scanning electron micrographs and acetylated-α-tubulin-LIR reveal that the proboscis and collar region are evenly covered with cilia, whereas on the trunk region, only scattered tufts of cilia are present (Fig. 5a, c).Fig. 5

Bottom Line: We found that all serotonin-like immunoreactive (LIR) neurons in both species are bipolar ciliary neurons that are intercalated between other epidermal cells.Unlike the tornaria larva of B. misakiensis, the embryonic nervous system of S. kowalevskii lacks serotonin-LIR neurons in the apical region as well as an opisthotroch neurite ring.Our data reveal a highly conserved mode of neurogenesis in enteropneusts that is independent of the developing mode and is inferred to be a common feature for Enteropneusta.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Zoology, University of Vienna, Althanstr. 14, 1090 Vienna, Austria.

ABSTRACT

Concerning the evolution of deuterostomes, enteropneusts (acorn worms) occupy a pivotal role as they share some characteristics with chordates (e.g., tunicates and vertebrates) but are also closely related to echinoderms (e.g., sea urchin). The nervous system in particular can be a highly informative organ system for evolutionary inferences, and advances in fluorescent microscopy have revealed overwhelming data sets on neurogenesis in various clades. However, immunocytochemical descriptions of neurogenesis of juvenile enteropneusts are particularly scarce, impeding the reconstruction of nervous system evolution in this group. We followed morphogenesis of the nervous system in two enteropneust species, one with direct (Saccoglossus kowalevskii) and the other with indirect development (Balanoglossus misakiensis), using an antibody against serotonin and electron microscopy. We found that all serotonin-like immunoreactive (LIR) neurons in both species are bipolar ciliary neurons that are intercalated between other epidermal cells. Unlike the tornaria larva of B. misakiensis, the embryonic nervous system of S. kowalevskii lacks serotonin-LIR neurons in the apical region as well as an opisthotroch neurite ring. Comparative analysis of both species shows that the projections of the serotonin-LIR somata initially form a basiepidermal plexus throughout the body that disappears within the trunk region soon after settlement before the concentrated dorsal and ventral neurite bundles emerge. Our data reveal a highly conserved mode of neurogenesis in enteropneusts that is independent of the developing mode and is inferred to be a common feature for Enteropneusta. Moreover, all detected serotonin-LIR neurons are presumably receptor cells, and the absence of serotonin-LIR interneurons from the enteropneust nervous system, which are otherwise common in various bilaterian central nervous systems, is interpreted as a loss that might have occurred already in the last common ancestor of Ambulacraria.

No MeSH data available.


Related in: MedlinePlus