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Myogenesis in the basal bilaterian Symsagittifera roscoffensis (Acoela).

Semmler H, Bailly X, Wanninger A - Front. Zool. (2008)

Bottom Line: In adult animals, the male gonopore with its associated sexual organs expresses distinct muscles.No specific statocyst muscles were found.In both juveniles and adults, non-muscular filaments, which stain positively for F-actin, are associated with certain sensory cells outside the bodywall musculature.

View Article: PubMed Central - HTML - PubMed

Affiliation: University of Copenhagen, Department of Biology, Research Group for Comparative Zoology, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark. hsemmler@bio.ku.dk.

ABSTRACT

Background: In order to increase the weak database concerning the organogenesis of Acoela - a clade regarded by many as the earliest extant offshoot of Bilateria and thus of particular interest for studies concerning the evolution of animal bodyplans - we analyzed the development of the musculature of Symsagittifera roscoffensis using F-actin labelling, confocal laserscanning microscopy, and 3D reconstruction software.

Results: At 40% of development between egg deposition and hatching short subepidermal fibres form. Muscle fibre development in the anterior body half precedes myogenesis in the posterior half. At 42% of development a grid of outer circular and inner longitudinal muscles is present in the bodywall. New circular muscles either branch off from present fibres or form adjacent to existing ones. The number of circular muscles is higher than that of the longitudinal muscles throughout all life cycle stages. Diagonal, circular and longitudinal muscles are initially rare but their number increases with time. The ventral side bears U-shaped muscles around the mouth, which in addition is surrounded by a sphincter muscle. With the exception of the region of the statocyst, dorsoventral muscles are present along the entire body of juveniles and adults, while adults additionally exhibit radially oriented internal muscles in the anterior tip. Outer diagonal muscles are present at the dorsal anterior tip of the adult. In adult animals, the male gonopore with its associated sexual organs expresses distinct muscles. No specific statocyst muscles were found. The muscle mantles of the needle-shaped sagittocysts are situated along the lateral edges of the animal and in the posterior end close to the male gonopore. In both juveniles and adults, non-muscular filaments, which stain positively for F-actin, are associated with certain sensory cells outside the bodywall musculature.

Conclusion: Compared to the myoanatomy of other acoel taxa, Symsagittifera roscoffensis shows a very complex musculature. Although data on presumably basal acoel clades are still scarce, the information currently available suggests an elaborated musculature with longitudinal, circular and U-shaped muscles as being part of the ancestral acoel bodyplan, thus increasing the possibility that Urbilateria likewise had a relatively complicated muscular ground pattern.

No MeSH data available.


Related in: MedlinePlus

CLSM micrographs of F-actin labelling in embryonic S. roscoffensis. A+B. Cleavage stages prior to muscle formation. Actin is expressed in the zonulae adhaerentes. A. 5 hours after egg deposition. B. 33 hours after egg deposition. The embryo possesses approximately 370 cells. C. 48 hours after egg deposition. Myogenesis in the anterior pole, facing upwards, precedes the development of muscle fibres in the posterior pole. Circular (cm), longitudinal (lm) and diagonal muscles (dm) are present. D-F. From the third day after egg deposition onwards, the ventral (D) and dorsal (E) sides are distinguishable. The anterior pole (asterisk) is surrounded by a spiral muscle. Additional muscles are formed by branching off from existing muscles (arrowheads). In addition, double-stranded muscles (double arrowheads) are present. F. Ventral anterior half of (D) in higher magnification. Scale bars: 50 μm.
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Figure 2: CLSM micrographs of F-actin labelling in embryonic S. roscoffensis. A+B. Cleavage stages prior to muscle formation. Actin is expressed in the zonulae adhaerentes. A. 5 hours after egg deposition. B. 33 hours after egg deposition. The embryo possesses approximately 370 cells. C. 48 hours after egg deposition. Myogenesis in the anterior pole, facing upwards, precedes the development of muscle fibres in the posterior pole. Circular (cm), longitudinal (lm) and diagonal muscles (dm) are present. D-F. From the third day after egg deposition onwards, the ventral (D) and dorsal (E) sides are distinguishable. The anterior pole (asterisk) is surrounded by a spiral muscle. Additional muscles are formed by branching off from existing muscles (arrowheads). In addition, double-stranded muscles (double arrowheads) are present. F. Ventral anterior half of (D) in higher magnification. Scale bars: 50 μm.

Mentions: In early cleavage stages, the zonulae adhaerentes of cells are stained with phalloidin (Figure 2A). 33 hours after egg deposition the embryo possesses about 370 cells. These cells have a diameter of about 10 μm and a penta- or hexagonal profile. On the third day (40–60% of development between egg deposition and hatching) an orthogonal muscle grid of longitudinal and circular muscles forms along the anterior-posterior axis of the embryo (Figures 2, 3 and 4), and few diagonal muscles become visible (Figure 2C). Short fibres form randomly basally to the epidermis at 40% of development between egg deposition and hatching. The anterior pole is surrounded by a spiral muscle fibre (Figure 2D, F), and the development of muscle fibres in the anterior half precedes myogenesis in the posterior half (Figure 2C–F). The establishment of the muscle grid seems more regular on the future ventral side than on the dorsal side (Figure 2D, E). Solid circular muscles are formed prior to the establishment of complete longitudinal muscles (Figure 2D–F). On the third day (approx. 50 hours and 42% of development between egg deposition and hatching), while a simple muscle grid is already established (Figure 3A), a concentration of actin is exhibited in the borders of surface cells (Figure 3B). Secondary circular muscles form by branching off from already existing circular muscles (Figures 2D–F and 3C) as well as by creating short double-stranded fibre zones, in which new fibres are formed adjacent to existing circular muscles (Figure 2E, F). Throughout the entire embryonic development more circular than longitudinal muscles are present. Accordingly, there are about 30 circular muscles and about 20 longitudinal muscles discernable at the third day after egg deposition (Figure 4). The solid muscle grid of the future ventral side appears more irregular than that of the dorsal side, which is caused by the presence of distinct muscles which probably are associated with the future mouth (Figure 4A and 4B versus 4C). On the dorsal side, the muscle grid is evenly distributed (Figures 4C and 5A, B). Internal muscles, which are dorso-ventrally orientated, are present at 72 hours (60% of development between egg deposition and hatching). Embryos with an age of about 85 hours (70% of development between egg deposition and hatching) show a ring muscle around the mouth.


Myogenesis in the basal bilaterian Symsagittifera roscoffensis (Acoela).

Semmler H, Bailly X, Wanninger A - Front. Zool. (2008)

CLSM micrographs of F-actin labelling in embryonic S. roscoffensis. A+B. Cleavage stages prior to muscle formation. Actin is expressed in the zonulae adhaerentes. A. 5 hours after egg deposition. B. 33 hours after egg deposition. The embryo possesses approximately 370 cells. C. 48 hours after egg deposition. Myogenesis in the anterior pole, facing upwards, precedes the development of muscle fibres in the posterior pole. Circular (cm), longitudinal (lm) and diagonal muscles (dm) are present. D-F. From the third day after egg deposition onwards, the ventral (D) and dorsal (E) sides are distinguishable. The anterior pole (asterisk) is surrounded by a spiral muscle. Additional muscles are formed by branching off from existing muscles (arrowheads). In addition, double-stranded muscles (double arrowheads) are present. F. Ventral anterior half of (D) in higher magnification. Scale bars: 50 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2562460&req=5

Figure 2: CLSM micrographs of F-actin labelling in embryonic S. roscoffensis. A+B. Cleavage stages prior to muscle formation. Actin is expressed in the zonulae adhaerentes. A. 5 hours after egg deposition. B. 33 hours after egg deposition. The embryo possesses approximately 370 cells. C. 48 hours after egg deposition. Myogenesis in the anterior pole, facing upwards, precedes the development of muscle fibres in the posterior pole. Circular (cm), longitudinal (lm) and diagonal muscles (dm) are present. D-F. From the third day after egg deposition onwards, the ventral (D) and dorsal (E) sides are distinguishable. The anterior pole (asterisk) is surrounded by a spiral muscle. Additional muscles are formed by branching off from existing muscles (arrowheads). In addition, double-stranded muscles (double arrowheads) are present. F. Ventral anterior half of (D) in higher magnification. Scale bars: 50 μm.
Mentions: In early cleavage stages, the zonulae adhaerentes of cells are stained with phalloidin (Figure 2A). 33 hours after egg deposition the embryo possesses about 370 cells. These cells have a diameter of about 10 μm and a penta- or hexagonal profile. On the third day (40–60% of development between egg deposition and hatching) an orthogonal muscle grid of longitudinal and circular muscles forms along the anterior-posterior axis of the embryo (Figures 2, 3 and 4), and few diagonal muscles become visible (Figure 2C). Short fibres form randomly basally to the epidermis at 40% of development between egg deposition and hatching. The anterior pole is surrounded by a spiral muscle fibre (Figure 2D, F), and the development of muscle fibres in the anterior half precedes myogenesis in the posterior half (Figure 2C–F). The establishment of the muscle grid seems more regular on the future ventral side than on the dorsal side (Figure 2D, E). Solid circular muscles are formed prior to the establishment of complete longitudinal muscles (Figure 2D–F). On the third day (approx. 50 hours and 42% of development between egg deposition and hatching), while a simple muscle grid is already established (Figure 3A), a concentration of actin is exhibited in the borders of surface cells (Figure 3B). Secondary circular muscles form by branching off from already existing circular muscles (Figures 2D–F and 3C) as well as by creating short double-stranded fibre zones, in which new fibres are formed adjacent to existing circular muscles (Figure 2E, F). Throughout the entire embryonic development more circular than longitudinal muscles are present. Accordingly, there are about 30 circular muscles and about 20 longitudinal muscles discernable at the third day after egg deposition (Figure 4). The solid muscle grid of the future ventral side appears more irregular than that of the dorsal side, which is caused by the presence of distinct muscles which probably are associated with the future mouth (Figure 4A and 4B versus 4C). On the dorsal side, the muscle grid is evenly distributed (Figures 4C and 5A, B). Internal muscles, which are dorso-ventrally orientated, are present at 72 hours (60% of development between egg deposition and hatching). Embryos with an age of about 85 hours (70% of development between egg deposition and hatching) show a ring muscle around the mouth.

Bottom Line: In adult animals, the male gonopore with its associated sexual organs expresses distinct muscles.No specific statocyst muscles were found.In both juveniles and adults, non-muscular filaments, which stain positively for F-actin, are associated with certain sensory cells outside the bodywall musculature.

View Article: PubMed Central - HTML - PubMed

Affiliation: University of Copenhagen, Department of Biology, Research Group for Comparative Zoology, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark. hsemmler@bio.ku.dk.

ABSTRACT

Background: In order to increase the weak database concerning the organogenesis of Acoela - a clade regarded by many as the earliest extant offshoot of Bilateria and thus of particular interest for studies concerning the evolution of animal bodyplans - we analyzed the development of the musculature of Symsagittifera roscoffensis using F-actin labelling, confocal laserscanning microscopy, and 3D reconstruction software.

Results: At 40% of development between egg deposition and hatching short subepidermal fibres form. Muscle fibre development in the anterior body half precedes myogenesis in the posterior half. At 42% of development a grid of outer circular and inner longitudinal muscles is present in the bodywall. New circular muscles either branch off from present fibres or form adjacent to existing ones. The number of circular muscles is higher than that of the longitudinal muscles throughout all life cycle stages. Diagonal, circular and longitudinal muscles are initially rare but their number increases with time. The ventral side bears U-shaped muscles around the mouth, which in addition is surrounded by a sphincter muscle. With the exception of the region of the statocyst, dorsoventral muscles are present along the entire body of juveniles and adults, while adults additionally exhibit radially oriented internal muscles in the anterior tip. Outer diagonal muscles are present at the dorsal anterior tip of the adult. In adult animals, the male gonopore with its associated sexual organs expresses distinct muscles. No specific statocyst muscles were found. The muscle mantles of the needle-shaped sagittocysts are situated along the lateral edges of the animal and in the posterior end close to the male gonopore. In both juveniles and adults, non-muscular filaments, which stain positively for F-actin, are associated with certain sensory cells outside the bodywall musculature.

Conclusion: Compared to the myoanatomy of other acoel taxa, Symsagittifera roscoffensis shows a very complex musculature. Although data on presumably basal acoel clades are still scarce, the information currently available suggests an elaborated musculature with longitudinal, circular and U-shaped muscles as being part of the ancestral acoel bodyplan, thus increasing the possibility that Urbilateria likewise had a relatively complicated muscular ground pattern.

No MeSH data available.


Related in: MedlinePlus