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Sponge budding is a spatiotemporal morphological patterning process: Insights from synchrotron radiation-based x-ray microtomography into the asexual reproduction of Tethya wilhelma.

Hammel JU, Herzen J, Beckmann F, Nickel M - Front. Zool. (2009)

Bottom Line: Based on morphometric data we defined four typical bud stages.Our results demonstrate that budding in demosponges is considerably more highly organized and regulated than previously assumed.Morphological pattern formation in asexual reproduction with underlying genetic regulation seems to have evolved early in metazoans and was likely part of the developmental program of the last common ancestor of all Metazoa (LCAM).

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut für Spezielle Zoologie und Evolutionsbiologie, Friedrich-Schiller-Universität Jena, Erbertstr, 1, 07743 Jena, Germany. m.nickel@uni-jena.de.

ABSTRACT

Background: Primary agametic-asexual reproduction mechanisms such as budding and fission are present in all non-bilaterian and many bilaterian animal taxa and are likely to be metazoan ground pattern characters. Cnidarians display highly organized and regulated budding processes. In contrast, budding in poriferans was thought to be less specific and related to the general ability of this group to reorganize their tissues. Here we test the hypothesis of morphological pattern formation during sponge budding.

Results: We investigated the budding process in Tethya wilhelma (Demospongiae) by applying 3D morphometrics to high resolution synchrotron radiation-based x-ray microtomography (SR-muCT) image data. We followed the morphogenesis of characteristic body structures and identified distinct morphological states which indeed reveal characteristic spatiotemporal morphological patterns in sponge bud development. We discovered the distribution of skeletal elements, canal system and sponge tissue to be based on a sequential series of distinct morphological states. Based on morphometric data we defined four typical bud stages. Once they have reached the final stage buds are released as fully functional juvenile sponges which are morphologically and functionally equivalent to adult specimens.

Conclusion: Our results demonstrate that budding in demosponges is considerably more highly organized and regulated than previously assumed. Morphological pattern formation in asexual reproduction with underlying genetic regulation seems to have evolved early in metazoans and was likely part of the developmental program of the last common ancestor of all Metazoa (LCAM).

No MeSH data available.


Related in: MedlinePlus

Detailed visualization and analysis of the overall morphology of a stage 4 T. wilhelma bud (data set E, see Additional file 2) based on SR μCT x-ray absorption and volumetric measurements. (A) Stereo pair rendering with segmentation of morphological structures: sponge tissue (yellow) separated into cortex (co) and choanoderm (cd) with developed choanocyte chambers (cc), exopinacoderm (exp), skeleton (red) and aquiferous system (blue) with lacunar system cavities (lsc). (B) Related volumetric measurements. Proportions [%] of sponge tissue, skeleton and aquiferous system measured on 1.4 μm slices. Proportional volume is given for all three spatial directions (x, y and z axes) and as xyz averages with standard deviations in relation to the sponge centre (x, y, z = 0,0,0 μm); arrows and lower case letters refer to C - N (slice images). Main body structures and body extensions (ext) are marked in grayscale. (C - N) examples of 1.4 μm slices in grayscale (left column) and colored x-ray absorption-based segmentation of morphological elements (right column). Two slices are presented per dataset direction: xy slices (C, D, I & J), zx slices (E, F, K & L), zy slices (G, H, M & N); lower case letters and lines in grayscale slice images mark the corresponding positions of the orthogonal planes shown as examples in C - N.
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Figure 2: Detailed visualization and analysis of the overall morphology of a stage 4 T. wilhelma bud (data set E, see Additional file 2) based on SR μCT x-ray absorption and volumetric measurements. (A) Stereo pair rendering with segmentation of morphological structures: sponge tissue (yellow) separated into cortex (co) and choanoderm (cd) with developed choanocyte chambers (cc), exopinacoderm (exp), skeleton (red) and aquiferous system (blue) with lacunar system cavities (lsc). (B) Related volumetric measurements. Proportions [%] of sponge tissue, skeleton and aquiferous system measured on 1.4 μm slices. Proportional volume is given for all three spatial directions (x, y and z axes) and as xyz averages with standard deviations in relation to the sponge centre (x, y, z = 0,0,0 μm); arrows and lower case letters refer to C - N (slice images). Main body structures and body extensions (ext) are marked in grayscale. (C - N) examples of 1.4 μm slices in grayscale (left column) and colored x-ray absorption-based segmentation of morphological elements (right column). Two slices are presented per dataset direction: xy slices (C, D, I & J), zx slices (E, F, K & L), zy slices (G, H, M & N); lower case letters and lines in grayscale slice images mark the corresponding positions of the orthogonal planes shown as examples in C - N.

Mentions: In order to present a detailed view of the main results of our qualitative and quantitative data analysis of SR-μCT datasets, this section makes available all the details of one dataset. Since late buds (which are already detached from the mother sponge) display a typical pattern of morphological structures, we have chosen dataset E (see Additional file 2) as an example. Mineral skeleton, aquiferous system and tissue compartment were analyzed. They were distinguished on the basis of their differing x-ray absorption characteristics (Fig. 2). All morphological elements of the sponge could be identified from the volumetric plot. In late buds we found an almost symmetrical arrangement of aquiferous system, tissue and skeleton along the three volume coordinate axes: x axis (= zy-slice stack), y axis (= zx-slice stack) and z axis (= xy-slice stacks) (Fig. 2B). The diameter of the specimen represents ~1000 μm. The coordinate axes are presented relative to the sponge center, thus ranging from -500 μm to +500 μm.


Sponge budding is a spatiotemporal morphological patterning process: Insights from synchrotron radiation-based x-ray microtomography into the asexual reproduction of Tethya wilhelma.

Hammel JU, Herzen J, Beckmann F, Nickel M - Front. Zool. (2009)

Detailed visualization and analysis of the overall morphology of a stage 4 T. wilhelma bud (data set E, see Additional file 2) based on SR μCT x-ray absorption and volumetric measurements. (A) Stereo pair rendering with segmentation of morphological structures: sponge tissue (yellow) separated into cortex (co) and choanoderm (cd) with developed choanocyte chambers (cc), exopinacoderm (exp), skeleton (red) and aquiferous system (blue) with lacunar system cavities (lsc). (B) Related volumetric measurements. Proportions [%] of sponge tissue, skeleton and aquiferous system measured on 1.4 μm slices. Proportional volume is given for all three spatial directions (x, y and z axes) and as xyz averages with standard deviations in relation to the sponge centre (x, y, z = 0,0,0 μm); arrows and lower case letters refer to C - N (slice images). Main body structures and body extensions (ext) are marked in grayscale. (C - N) examples of 1.4 μm slices in grayscale (left column) and colored x-ray absorption-based segmentation of morphological elements (right column). Two slices are presented per dataset direction: xy slices (C, D, I & J), zx slices (E, F, K & L), zy slices (G, H, M & N); lower case letters and lines in grayscale slice images mark the corresponding positions of the orthogonal planes shown as examples in C - N.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2749020&req=5

Figure 2: Detailed visualization and analysis of the overall morphology of a stage 4 T. wilhelma bud (data set E, see Additional file 2) based on SR μCT x-ray absorption and volumetric measurements. (A) Stereo pair rendering with segmentation of morphological structures: sponge tissue (yellow) separated into cortex (co) and choanoderm (cd) with developed choanocyte chambers (cc), exopinacoderm (exp), skeleton (red) and aquiferous system (blue) with lacunar system cavities (lsc). (B) Related volumetric measurements. Proportions [%] of sponge tissue, skeleton and aquiferous system measured on 1.4 μm slices. Proportional volume is given for all three spatial directions (x, y and z axes) and as xyz averages with standard deviations in relation to the sponge centre (x, y, z = 0,0,0 μm); arrows and lower case letters refer to C - N (slice images). Main body structures and body extensions (ext) are marked in grayscale. (C - N) examples of 1.4 μm slices in grayscale (left column) and colored x-ray absorption-based segmentation of morphological elements (right column). Two slices are presented per dataset direction: xy slices (C, D, I & J), zx slices (E, F, K & L), zy slices (G, H, M & N); lower case letters and lines in grayscale slice images mark the corresponding positions of the orthogonal planes shown as examples in C - N.
Mentions: In order to present a detailed view of the main results of our qualitative and quantitative data analysis of SR-μCT datasets, this section makes available all the details of one dataset. Since late buds (which are already detached from the mother sponge) display a typical pattern of morphological structures, we have chosen dataset E (see Additional file 2) as an example. Mineral skeleton, aquiferous system and tissue compartment were analyzed. They were distinguished on the basis of their differing x-ray absorption characteristics (Fig. 2). All morphological elements of the sponge could be identified from the volumetric plot. In late buds we found an almost symmetrical arrangement of aquiferous system, tissue and skeleton along the three volume coordinate axes: x axis (= zy-slice stack), y axis (= zx-slice stack) and z axis (= xy-slice stacks) (Fig. 2B). The diameter of the specimen represents ~1000 μm. The coordinate axes are presented relative to the sponge center, thus ranging from -500 μm to +500 μm.

Bottom Line: Based on morphometric data we defined four typical bud stages.Our results demonstrate that budding in demosponges is considerably more highly organized and regulated than previously assumed.Morphological pattern formation in asexual reproduction with underlying genetic regulation seems to have evolved early in metazoans and was likely part of the developmental program of the last common ancestor of all Metazoa (LCAM).

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut für Spezielle Zoologie und Evolutionsbiologie, Friedrich-Schiller-Universität Jena, Erbertstr, 1, 07743 Jena, Germany. m.nickel@uni-jena.de.

ABSTRACT

Background: Primary agametic-asexual reproduction mechanisms such as budding and fission are present in all non-bilaterian and many bilaterian animal taxa and are likely to be metazoan ground pattern characters. Cnidarians display highly organized and regulated budding processes. In contrast, budding in poriferans was thought to be less specific and related to the general ability of this group to reorganize their tissues. Here we test the hypothesis of morphological pattern formation during sponge budding.

Results: We investigated the budding process in Tethya wilhelma (Demospongiae) by applying 3D morphometrics to high resolution synchrotron radiation-based x-ray microtomography (SR-muCT) image data. We followed the morphogenesis of characteristic body structures and identified distinct morphological states which indeed reveal characteristic spatiotemporal morphological patterns in sponge bud development. We discovered the distribution of skeletal elements, canal system and sponge tissue to be based on a sequential series of distinct morphological states. Based on morphometric data we defined four typical bud stages. Once they have reached the final stage buds are released as fully functional juvenile sponges which are morphologically and functionally equivalent to adult specimens.

Conclusion: Our results demonstrate that budding in demosponges is considerably more highly organized and regulated than previously assumed. Morphological pattern formation in asexual reproduction with underlying genetic regulation seems to have evolved early in metazoans and was likely part of the developmental program of the last common ancestor of all Metazoa (LCAM).

No MeSH data available.


Related in: MedlinePlus