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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 medusa marginal tentacle in Aurelia sp.1.All scale bars equal 50 μm. (A) Illustration of a longitudinal section of the medusa marginal tentacle in Aurelia. (B) Phalloidin staining of three marginal tentacles (upper left proximal, lower right distal), which elucidate the muscle chord running down the oral side of each tentacle. A single tentacle has been digitally isolated using Adobe Photoshop in the upper-right box (left proximal, bottom oral) to clarify the distinction between the proximal “blade” (bl) and distal “constriction” (co). (C) Confocal longitudinal section of the marginal tentacle, showing where the proximal “blade” changes into the radially symmetrical distal “constriction”. (D) Another confocal longitudinal section, highlighting the dense packing of endodermal (en) cells in the distal portion of the tentacle. Note the distinction between this morphology and the chordal morphology seen in the polyp (Fig 2A and 2B). (E) Z-projection illustrating the modular clusters of cells in the distal portion of the marginal tentacle. (F) A longitudinal section of Fig 3E. (G) A Z-projection of phalloidin staining in Fig 3E. Note in (F) and (G) that phalloidin bands do not appear to generate cohesive longitudinal musculature, but instead form localized musculature within each module (H) Low-magnification image of neural distribution across the medusa bell. Arrowheads indicate putative clusters of Ttub-positive neurites. (I) High magnification of the proximal-most end of the tentacle, showing FMRFamide and Ttub-positive neurites associated with the muscle chord. (J) A Z-projection revealing the high concentration of “capsule”-positive cnidocytes in the tentacle ectoderm. (K) A partially fired cnidocyte from 2J (white box), digitally isolated using Adobe Photoshop. (L) Longitudinal TEM section of a microbasic heterotrichous eurytele (X 9,000).
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pone.0134741.g003: Morphology of the medusa marginal tentacle in Aurelia sp.1.All scale bars equal 50 μm. (A) Illustration of a longitudinal section of the medusa marginal tentacle in Aurelia. (B) Phalloidin staining of three marginal tentacles (upper left proximal, lower right distal), which elucidate the muscle chord running down the oral side of each tentacle. A single tentacle has been digitally isolated using Adobe Photoshop in the upper-right box (left proximal, bottom oral) to clarify the distinction between the proximal “blade” (bl) and distal “constriction” (co). (C) Confocal longitudinal section of the marginal tentacle, showing where the proximal “blade” changes into the radially symmetrical distal “constriction”. (D) Another confocal longitudinal section, highlighting the dense packing of endodermal (en) cells in the distal portion of the tentacle. Note the distinction between this morphology and the chordal morphology seen in the polyp (Fig 2A and 2B). (E) Z-projection illustrating the modular clusters of cells in the distal portion of the marginal tentacle. (F) A longitudinal section of Fig 3E. (G) A Z-projection of phalloidin staining in Fig 3E. Note in (F) and (G) that phalloidin bands do not appear to generate cohesive longitudinal musculature, but instead form localized musculature within each module (H) Low-magnification image of neural distribution across the medusa bell. Arrowheads indicate putative clusters of Ttub-positive neurites. (I) High magnification of the proximal-most end of the tentacle, showing FMRFamide and Ttub-positive neurites associated with the muscle chord. (J) A Z-projection revealing the high concentration of “capsule”-positive cnidocytes in the tentacle ectoderm. (K) A partially fired cnidocyte from 2J (white box), digitally isolated using Adobe Photoshop. (L) Longitudinal TEM section of a microbasic heterotrichous eurytele (X 9,000).

Mentions: 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).


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 medusa marginal tentacle in Aurelia sp.1.All scale bars equal 50 μm. (A) Illustration of a longitudinal section of the medusa marginal tentacle in Aurelia. (B) Phalloidin staining of three marginal tentacles (upper left proximal, lower right distal), which elucidate the muscle chord running down the oral side of each tentacle. A single tentacle has been digitally isolated using Adobe Photoshop in the upper-right box (left proximal, bottom oral) to clarify the distinction between the proximal “blade” (bl) and distal “constriction” (co). (C) Confocal longitudinal section of the marginal tentacle, showing where the proximal “blade” changes into the radially symmetrical distal “constriction”. (D) Another confocal longitudinal section, highlighting the dense packing of endodermal (en) cells in the distal portion of the tentacle. Note the distinction between this morphology and the chordal morphology seen in the polyp (Fig 2A and 2B). (E) Z-projection illustrating the modular clusters of cells in the distal portion of the marginal tentacle. (F) A longitudinal section of Fig 3E. (G) A Z-projection of phalloidin staining in Fig 3E. Note in (F) and (G) that phalloidin bands do not appear to generate cohesive longitudinal musculature, but instead form localized musculature within each module (H) Low-magnification image of neural distribution across the medusa bell. Arrowheads indicate putative clusters of Ttub-positive neurites. (I) High magnification of the proximal-most end of the tentacle, showing FMRFamide and Ttub-positive neurites associated with the muscle chord. (J) A Z-projection revealing the high concentration of “capsule”-positive cnidocytes in the tentacle ectoderm. (K) A partially fired cnidocyte from 2J (white box), digitally isolated using Adobe Photoshop. (L) Longitudinal TEM section of a microbasic heterotrichous eurytele (X 9,000).
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pone.0134741.g003: Morphology of the medusa marginal tentacle in Aurelia sp.1.All scale bars equal 50 μm. (A) Illustration of a longitudinal section of the medusa marginal tentacle in Aurelia. (B) Phalloidin staining of three marginal tentacles (upper left proximal, lower right distal), which elucidate the muscle chord running down the oral side of each tentacle. A single tentacle has been digitally isolated using Adobe Photoshop in the upper-right box (left proximal, bottom oral) to clarify the distinction between the proximal “blade” (bl) and distal “constriction” (co). (C) Confocal longitudinal section of the marginal tentacle, showing where the proximal “blade” changes into the radially symmetrical distal “constriction”. (D) Another confocal longitudinal section, highlighting the dense packing of endodermal (en) cells in the distal portion of the tentacle. Note the distinction between this morphology and the chordal morphology seen in the polyp (Fig 2A and 2B). (E) Z-projection illustrating the modular clusters of cells in the distal portion of the marginal tentacle. (F) A longitudinal section of Fig 3E. (G) A Z-projection of phalloidin staining in Fig 3E. Note in (F) and (G) that phalloidin bands do not appear to generate cohesive longitudinal musculature, but instead form localized musculature within each module (H) Low-magnification image of neural distribution across the medusa bell. Arrowheads indicate putative clusters of Ttub-positive neurites. (I) High magnification of the proximal-most end of the tentacle, showing FMRFamide and Ttub-positive neurites associated with the muscle chord. (J) A Z-projection revealing the high concentration of “capsule”-positive cnidocytes in the tentacle ectoderm. (K) A partially fired cnidocyte from 2J (white box), digitally isolated using Adobe Photoshop. (L) Longitudinal TEM section of a microbasic heterotrichous eurytele (X 9,000).
Mentions: 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).

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