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Structural and Developmental Disparity in the Tentacles of the Moon Jellyfish Aurelia sp.1.

Gold DA, Nakanishi N, Hensley NM, Cozzolino K, Tabatabaee M, Martin M, Hartenstein V, Jacobs DK - PLoS ONE (2015)

Bottom Line: While cnidarian tentacles are generally characterized as structures evolved for feeding and defense, significant variation exists between the tentacles of different species, and within the same species across different life stages and/or body regions.We show that polyp oral tentacles and medusa marginal tentacles display markedly different cellular and muscular architecture, as well as distinct patterns of cellular proliferation during growth.However, differences in cell proliferation dynamics suggests that the two tentacle forms lack a conserved mechanism of development, challenging the textbook-notion that cnidarian tentacles can be homologized into a conserved bauplan.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biolology. University of California Los Angeles, Los Angeles, California, United States of America.

ABSTRACT
Tentacles armed with stinging cells (cnidocytes) are a defining trait of the cnidarians, a phylum that includes sea anemones, corals, jellyfish, and hydras. While cnidarian tentacles are generally characterized as structures evolved for feeding and defense, significant variation exists between the tentacles of different species, and within the same species across different life stages and/or body regions. Such diversity suggests cryptic distinctions exist in tentacle function. In this paper, we use confocal and transmission electron microscopy to contrast the structure and development of tentacles in the moon jellyfish, Aurelia species 1. We show that polyp oral tentacles and medusa marginal tentacles display markedly different cellular and muscular architecture, as well as distinct patterns of cellular proliferation during growth. Many structural differences between these tentacle types may reflect biomechanical solutions to different feeding strategies, although further work would be required for a precise mechanistic understanding. However, differences in cell proliferation dynamics suggests that the two tentacle forms lack a conserved mechanism of development, challenging the textbook-notion that cnidarian tentacles can be homologized into a conserved bauplan.

No MeSH data available.


Related in: MedlinePlus

Morphology of the polyp oral tentacle in Aurelia sp.1.All scale bars represent 50 μm. (A) Longitudinal section of tentacle, revealing the morphology and distribution of ectodermal (ec) and endodermal (en) cells. (B) A similar image showing the distribution of nuclei in the tentacle. Note the row of large, vacuolated cells in the endoderm. (C) Longitudinal section demonstrating how anti-Ttub can be used to identify cnidocytes. Examples where enlarged cells (caused by the presence of the cnidocyte capsule) are co-localized with crescent-shaped nuclei are labeled with arrows. (D) Phalloidin staining at the base of a tentacle. (E) A partial stack of confocal images, revealing the circumferential myofibrils (Cm) underneath the longitudinal musculature of the epitheliomuscular cells. (F) A partial stack of confocal images deeper in the longitudinal section, which suggests that space (presumably mesoglea) separates the longitudinal and radial musculature. (G) TEM of an oblique longitudinal cut on the polyp tentacle, producing a peninsula of tissue rich in longitudinal myofibrils (Lm) situated above the vacuolated space (Vac) of an endodermal cell. (H) Close-up of the box in Fig 1G, clarifying longitudinal myofibrils (Lm), circumferential myofibrils (Cm), and mesoglea (Me). (I) Distribution of anti-FMRFamide-positive neurons and their processes. (J) Co-labeling of anti-FMRFamide and anti-Ttub. Note how anti-Ttub labels additional neural tracts that are not FMRF-positive. (K) Distribution of anti-Ttub and “capsule” positive cells. In these images, the antibody labels the apical tip of most cells; which is distinct from the cnidocyte specific expression found in the planula or medusa (see Fig 3J). (L) Longitudinal TEM section of several atrichous isorhizas (X 17,000). (M) Longitudinal TEM section of a microbasic heterotrichous eurytele (X 17,000).
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pone.0134741.g002: Morphology of the polyp oral tentacle in Aurelia sp.1.All scale bars represent 50 μm. (A) Longitudinal section of tentacle, revealing the morphology and distribution of ectodermal (ec) and endodermal (en) cells. (B) A similar image showing the distribution of nuclei in the tentacle. Note the row of large, vacuolated cells in the endoderm. (C) Longitudinal section demonstrating how anti-Ttub can be used to identify cnidocytes. Examples where enlarged cells (caused by the presence of the cnidocyte capsule) are co-localized with crescent-shaped nuclei are labeled with arrows. (D) Phalloidin staining at the base of a tentacle. (E) A partial stack of confocal images, revealing the circumferential myofibrils (Cm) underneath the longitudinal musculature of the epitheliomuscular cells. (F) A partial stack of confocal images deeper in the longitudinal section, which suggests that space (presumably mesoglea) separates the longitudinal and radial musculature. (G) TEM of an oblique longitudinal cut on the polyp tentacle, producing a peninsula of tissue rich in longitudinal myofibrils (Lm) situated above the vacuolated space (Vac) of an endodermal cell. (H) Close-up of the box in Fig 1G, clarifying longitudinal myofibrils (Lm), circumferential myofibrils (Cm), and mesoglea (Me). (I) Distribution of anti-FMRFamide-positive neurons and their processes. (J) Co-labeling of anti-FMRFamide and anti-Ttub. Note how anti-Ttub labels additional neural tracts that are not FMRF-positive. (K) Distribution of anti-Ttub and “capsule” positive cells. In these images, the antibody labels the apical tip of most cells; which is distinct from the cnidocyte specific expression found in the planula or medusa (see Fig 3J). (L) Longitudinal TEM section of several atrichous isorhizas (X 17,000). (M) Longitudinal TEM section of a microbasic heterotrichous eurytele (X 17,000).

Mentions: In the developing polyp, four tentacles bud around the mouth; additional tentacles intercalate between developing ones, until sixteen are formed [21]. Oral tentacles are of the solid (or chordal) variety, with a single row of large, highly vacuolated cells filling the endoderm [2,18,23] (Fig 2A and 2B). The ectoderm consists primarily of epitheliomuscular cells, neurons, gland cells and cnidocytes. Based on TEM data, Chia, Amerongen, and Peteya [23] suggest that the tentacle ectoderm can be divided into a superficial epithelial and subepithelial layer. However, such layering is probably a consequence of tentacle retraction; in extended (relaxed) tentacles, nuclear staining suggests that the ectoderm is rarely more than one cell deep (Fig 2B). Epitheliomuscular cells are apically ciliated (Fig 2A), and project basal myofibrils that generate the longitudinal musculature of the tentacle (Fig 2A–2C). We did not find an asymmetric concentration of longitudinal musculature at the proximal end of the tentacle (Fig 2D), as had been reported previously [23].


Structural and Developmental Disparity in the Tentacles of the Moon Jellyfish Aurelia sp.1.

Gold DA, Nakanishi N, Hensley NM, Cozzolino K, Tabatabaee M, Martin M, Hartenstein V, Jacobs DK - PLoS ONE (2015)

Morphology of the polyp oral tentacle in Aurelia sp.1.All scale bars represent 50 μm. (A) Longitudinal section of tentacle, revealing the morphology and distribution of ectodermal (ec) and endodermal (en) cells. (B) A similar image showing the distribution of nuclei in the tentacle. Note the row of large, vacuolated cells in the endoderm. (C) Longitudinal section demonstrating how anti-Ttub can be used to identify cnidocytes. Examples where enlarged cells (caused by the presence of the cnidocyte capsule) are co-localized with crescent-shaped nuclei are labeled with arrows. (D) Phalloidin staining at the base of a tentacle. (E) A partial stack of confocal images, revealing the circumferential myofibrils (Cm) underneath the longitudinal musculature of the epitheliomuscular cells. (F) A partial stack of confocal images deeper in the longitudinal section, which suggests that space (presumably mesoglea) separates the longitudinal and radial musculature. (G) TEM of an oblique longitudinal cut on the polyp tentacle, producing a peninsula of tissue rich in longitudinal myofibrils (Lm) situated above the vacuolated space (Vac) of an endodermal cell. (H) Close-up of the box in Fig 1G, clarifying longitudinal myofibrils (Lm), circumferential myofibrils (Cm), and mesoglea (Me). (I) Distribution of anti-FMRFamide-positive neurons and their processes. (J) Co-labeling of anti-FMRFamide and anti-Ttub. Note how anti-Ttub labels additional neural tracts that are not FMRF-positive. (K) Distribution of anti-Ttub and “capsule” positive cells. In these images, the antibody labels the apical tip of most cells; which is distinct from the cnidocyte specific expression found in the planula or medusa (see Fig 3J). (L) Longitudinal TEM section of several atrichous isorhizas (X 17,000). (M) Longitudinal TEM section of a microbasic heterotrichous eurytele (X 17,000).
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Related In: Results  -  Collection

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pone.0134741.g002: Morphology of the polyp oral tentacle in Aurelia sp.1.All scale bars represent 50 μm. (A) Longitudinal section of tentacle, revealing the morphology and distribution of ectodermal (ec) and endodermal (en) cells. (B) A similar image showing the distribution of nuclei in the tentacle. Note the row of large, vacuolated cells in the endoderm. (C) Longitudinal section demonstrating how anti-Ttub can be used to identify cnidocytes. Examples where enlarged cells (caused by the presence of the cnidocyte capsule) are co-localized with crescent-shaped nuclei are labeled with arrows. (D) Phalloidin staining at the base of a tentacle. (E) A partial stack of confocal images, revealing the circumferential myofibrils (Cm) underneath the longitudinal musculature of the epitheliomuscular cells. (F) A partial stack of confocal images deeper in the longitudinal section, which suggests that space (presumably mesoglea) separates the longitudinal and radial musculature. (G) TEM of an oblique longitudinal cut on the polyp tentacle, producing a peninsula of tissue rich in longitudinal myofibrils (Lm) situated above the vacuolated space (Vac) of an endodermal cell. (H) Close-up of the box in Fig 1G, clarifying longitudinal myofibrils (Lm), circumferential myofibrils (Cm), and mesoglea (Me). (I) Distribution of anti-FMRFamide-positive neurons and their processes. (J) Co-labeling of anti-FMRFamide and anti-Ttub. Note how anti-Ttub labels additional neural tracts that are not FMRF-positive. (K) Distribution of anti-Ttub and “capsule” positive cells. In these images, the antibody labels the apical tip of most cells; which is distinct from the cnidocyte specific expression found in the planula or medusa (see Fig 3J). (L) Longitudinal TEM section of several atrichous isorhizas (X 17,000). (M) Longitudinal TEM section of a microbasic heterotrichous eurytele (X 17,000).
Mentions: In the developing polyp, four tentacles bud around the mouth; additional tentacles intercalate between developing ones, until sixteen are formed [21]. Oral tentacles are of the solid (or chordal) variety, with a single row of large, highly vacuolated cells filling the endoderm [2,18,23] (Fig 2A and 2B). The ectoderm consists primarily of epitheliomuscular cells, neurons, gland cells and cnidocytes. Based on TEM data, Chia, Amerongen, and Peteya [23] suggest that the tentacle ectoderm can be divided into a superficial epithelial and subepithelial layer. However, such layering is probably a consequence of tentacle retraction; in extended (relaxed) tentacles, nuclear staining suggests that the ectoderm is rarely more than one cell deep (Fig 2B). Epitheliomuscular cells are apically ciliated (Fig 2A), and project basal myofibrils that generate the longitudinal musculature of the tentacle (Fig 2A–2C). We did not find an asymmetric concentration of longitudinal musculature at the proximal end of the tentacle (Fig 2D), as had been reported previously [23].

Bottom Line: While cnidarian tentacles are generally characterized as structures evolved for feeding and defense, significant variation exists between the tentacles of different species, and within the same species across different life stages and/or body regions.We show that polyp oral tentacles and medusa marginal tentacles display markedly different cellular and muscular architecture, as well as distinct patterns of cellular proliferation during growth.However, differences in cell proliferation dynamics suggests that the two tentacle forms lack a conserved mechanism of development, challenging the textbook-notion that cnidarian tentacles can be homologized into a conserved bauplan.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biolology. University of California Los Angeles, Los Angeles, California, United States of America.

ABSTRACT
Tentacles armed with stinging cells (cnidocytes) are a defining trait of the cnidarians, a phylum that includes sea anemones, corals, jellyfish, and hydras. While cnidarian tentacles are generally characterized as structures evolved for feeding and defense, significant variation exists between the tentacles of different species, and within the same species across different life stages and/or body regions. Such diversity suggests cryptic distinctions exist in tentacle function. In this paper, we use confocal and transmission electron microscopy to contrast the structure and development of tentacles in the moon jellyfish, Aurelia species 1. We show that polyp oral tentacles and medusa marginal tentacles display markedly different cellular and muscular architecture, as well as distinct patterns of cellular proliferation during growth. Many structural differences between these tentacle types may reflect biomechanical solutions to different feeding strategies, although further work would be required for a precise mechanistic understanding. However, differences in cell proliferation dynamics suggests that the two tentacle forms lack a conserved mechanism of development, challenging the textbook-notion that cnidarian tentacles can be homologized into a conserved bauplan.

No MeSH data available.


Related in: MedlinePlus