Development and myogenesis of the vermiform <it>Buddenbrockia</it> (Myxozoa) and implications for cnidarian body plan evolution

<p>Abstract</p> <p>Background</p> <p>The enigmatic wormlike parasite <it>Buddenbrockia plumatellae</it> has recently been shown to belong to the Myxozoa, which are now supported as a clade within Cnidaria. Most myxozoans are morphologically extremely simplif...

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Main Authors: Gruhl Alexander, Okamura Beth
Format: Article
Language:English
Published: BMC 2012-05-01
Series:EvoDevo
Subjects:
Online Access:http://www.evodevojournal.com/content/3/1/10
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spelling doaj-efc2f37ac90448cc8ccd0f6bf05592642020-11-24T22:21:03ZengBMCEvoDevo2041-91392012-05-01311010.1186/2041-9139-3-10Development and myogenesis of the vermiform <it>Buddenbrockia</it> (Myxozoa) and implications for cnidarian body plan evolutionGruhl AlexanderOkamura Beth<p>Abstract</p> <p>Background</p> <p>The enigmatic wormlike parasite <it>Buddenbrockia plumatellae</it> has recently been shown to belong to the Myxozoa, which are now supported as a clade within Cnidaria. Most myxozoans are morphologically extremely simplified, lacking major metazoan features such as epithelial tissue layers, gut, nervous system, body axes and gonads. This hinders comparisons to free-living cnidarians and thus an understanding of myxozoan evolution and identification of their cnidarian sister group. However, <it>B. plumatellae</it> is less simplified than other myxozoans and therefore is of specific significance for such evolutionary considerations.</p> <p>Methods</p> <p>We analyse and describe the development of major body plan features in <it>Buddenbrockia</it> worms using a combination of histology, electron microscopy and confocal microscopy.</p> <p>Results</p> <p>Early developmental stages develop a primary body axis that shows a polarity, which is manifested as a gradient of tissue development, enabling distinction between the two worm tips. This polarity is maintained in adult worms, which, in addition, often develop a pore at the distal tip. The musculature comprises tetraradially arranged longitudinal muscle blocks consisting of independent myocytes embedded in the extracellular matrix between inner and outer epithelial tissue layers. The muscle fibres are obliquely oriented and in fully grown worms consistently form an angle of 12° with respect to the longitudinal axis of the worm in each muscle block and hence confer chirality. Connecting cells form a link between each muscle block and constitute four rows of cells that run in single file along the length of the worm. These connecting cells are remnants of the inner epithelial tissue layer and are anchored to the extracellular matrix. They are likely to have a biomechanical function.</p> <p>Conclusions</p> <p>The polarised primary body axis represents an ancient feature present in the last common ancestor of Cnidaria and Bilateria. The tetraradial arrangement of musculature is consistent with a medusozoan affinity for Myxozoa. However, the chiral pattern of muscle fibre orientation is apparently novel within Cnidaria and could thus be a specific adaptation. The presence of independent myocytes instead of Cnidaria-like epitheliomuscular cells can be interpreted as further support for the presence of mesoderm in cnidarians, or it may represent convergent evolution to a bilaterian condition.</p> http://www.evodevojournal.com/content/3/1/10CnidariaMyxozoa<it>Buddenbrockia</it>EndoparasitismDevelopmentBody axesSymmetryChiralityMusculatureMesoderm
collection DOAJ
language English
format Article
sources DOAJ
author Gruhl Alexander
Okamura Beth
spellingShingle Gruhl Alexander
Okamura Beth
Development and myogenesis of the vermiform <it>Buddenbrockia</it> (Myxozoa) and implications for cnidarian body plan evolution
EvoDevo
Cnidaria
Myxozoa
<it>Buddenbrockia</it>
Endoparasitism
Development
Body axes
Symmetry
Chirality
Musculature
Mesoderm
author_facet Gruhl Alexander
Okamura Beth
author_sort Gruhl Alexander
title Development and myogenesis of the vermiform <it>Buddenbrockia</it> (Myxozoa) and implications for cnidarian body plan evolution
title_short Development and myogenesis of the vermiform <it>Buddenbrockia</it> (Myxozoa) and implications for cnidarian body plan evolution
title_full Development and myogenesis of the vermiform <it>Buddenbrockia</it> (Myxozoa) and implications for cnidarian body plan evolution
title_fullStr Development and myogenesis of the vermiform <it>Buddenbrockia</it> (Myxozoa) and implications for cnidarian body plan evolution
title_full_unstemmed Development and myogenesis of the vermiform <it>Buddenbrockia</it> (Myxozoa) and implications for cnidarian body plan evolution
title_sort development and myogenesis of the vermiform <it>buddenbrockia</it> (myxozoa) and implications for cnidarian body plan evolution
publisher BMC
series EvoDevo
issn 2041-9139
publishDate 2012-05-01
description <p>Abstract</p> <p>Background</p> <p>The enigmatic wormlike parasite <it>Buddenbrockia plumatellae</it> has recently been shown to belong to the Myxozoa, which are now supported as a clade within Cnidaria. Most myxozoans are morphologically extremely simplified, lacking major metazoan features such as epithelial tissue layers, gut, nervous system, body axes and gonads. This hinders comparisons to free-living cnidarians and thus an understanding of myxozoan evolution and identification of their cnidarian sister group. However, <it>B. plumatellae</it> is less simplified than other myxozoans and therefore is of specific significance for such evolutionary considerations.</p> <p>Methods</p> <p>We analyse and describe the development of major body plan features in <it>Buddenbrockia</it> worms using a combination of histology, electron microscopy and confocal microscopy.</p> <p>Results</p> <p>Early developmental stages develop a primary body axis that shows a polarity, which is manifested as a gradient of tissue development, enabling distinction between the two worm tips. This polarity is maintained in adult worms, which, in addition, often develop a pore at the distal tip. The musculature comprises tetraradially arranged longitudinal muscle blocks consisting of independent myocytes embedded in the extracellular matrix between inner and outer epithelial tissue layers. The muscle fibres are obliquely oriented and in fully grown worms consistently form an angle of 12° with respect to the longitudinal axis of the worm in each muscle block and hence confer chirality. Connecting cells form a link between each muscle block and constitute four rows of cells that run in single file along the length of the worm. These connecting cells are remnants of the inner epithelial tissue layer and are anchored to the extracellular matrix. They are likely to have a biomechanical function.</p> <p>Conclusions</p> <p>The polarised primary body axis represents an ancient feature present in the last common ancestor of Cnidaria and Bilateria. The tetraradial arrangement of musculature is consistent with a medusozoan affinity for Myxozoa. However, the chiral pattern of muscle fibre orientation is apparently novel within Cnidaria and could thus be a specific adaptation. The presence of independent myocytes instead of Cnidaria-like epitheliomuscular cells can be interpreted as further support for the presence of mesoderm in cnidarians, or it may represent convergent evolution to a bilaterian condition.</p>
topic Cnidaria
Myxozoa
<it>Buddenbrockia</it>
Endoparasitism
Development
Body axes
Symmetry
Chirality
Musculature
Mesoderm
url http://www.evodevojournal.com/content/3/1/10
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