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Electron tomographic analysis of cytokinesis in the brown alga Silvetia babingtonii (Fucales, Phaeophyceae)

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Abstract

In brown algae, membrane resources for the new cell partition during cytokinesis are mainly flat cisternae (FCs) and Golgi-derived vesicles. We used electron tomography coupled with rapid freezing/freeze substitution of zygotes to clarify the structure of transient membrane compartments during cytokinesis in Silvetia zygotes. After mitosis, an amorphous membranous structure, considered to be an FC intermediate was observed near endoplasmic reticulum clusters, lying between two daughter nuclei. FCs were arrayed at the cytokinetic plane, and a tubular membranous network was formed around them. This network might be formed by the consecutive fusion of spherical vesicles that are linked to the edges of FCs to form a membranous network (MN). At the initial stage of the formation of a membranous sac (MS) from the MN, the MS had flat and swollen parts, with the latter showing membranous tunnels. Coated pits were detected with high frequency at the swollen parts of the MS. This observation indicated that membranous tunnels disappeared by recycling of excess membrane via endocytosis, and the swollen part became flat. The MN appeared at the edges of the growing MS. MN and the MN-MS complex were observed along the cytokinetic plane in several spaces. The MS expanded by the incorporation of MN or other MS in its neighborhood. With the maturation of the new cell partition membrane, the thickness of the MS became constant and the membrane cavity disappeared. The changes in the surface area and volume of the transient membrane compartment during cytokinesis were analyzed from the tomographic data.

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Acknowledgments

This study was supported by the JSPS KAKENHI grant numbers 21770065, 22370034, and 25291087. This work was supported by the Nanotechnology Network Project of the Ministry of Education, Culture, Sports, Science and Technology, Japan, at the Research Center for Ultrahigh Voltage Electron Microscopy, Osaka University (Handai multi-functional Nano-Foundry). We thank Dr. M. Takeuchi from the University of Tokyo for the technical advice.

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Muroran Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Muroran, 051-0013, Japan

    Chikako Nagasato & Taizo Motomura

  2. Graduate School of Frontier Biosciences, Osaka University, 1-3 Yamadaoka, Suita, Osaka, 565-0871, Japan

    Naoko Kajimura

  3. JEOL Ltd, 5-14-5 Nishinakajima, Yodogawa-ku, Osaka, 532-0011, Japan

    Naoko Kajimura

  4. Graduate School of Environmental Science, Hokkaido University, Sapporo, 060-0810, Japan

    Makoto Terauchi

  5. Department of Science, Graduate School of Life Science, University of Hyogo, 2167 Shosha, Himeji, Hyogo, 671-2280, Japan

    Yoshinobu Mineyuki

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  1. Chikako Nagasato
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Correspondence to Chikako Nagasato.

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Electronic supplementary material

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A sequence of 1.54 nm-thick tomographic slices shown in Figure 2. (MP4 2862 kb)

A sequence of 2.24 nm-thick tomographic slices shown in Figure 5. (MP4 2639 kb)

Supplement Figure 1

Three-dimensional model from tomography shown in Figure 3. The dark vesicle (pale pink), flat cisterna (FC; green), light vesicle (yellow), membranous sac (MS; pink) and TN (dark pink) are depicted. Membranous network (MN) indicates TN and FCs connected with it. Scale bar, 500 nm. (JPEG 5 kb)

High Resolution Image (TIFF 3157 kb)

Supplement Figure 2

Three-dimensional model from tomography shown in Figure 5. The coated pit (CP; blue), dark vesicle (pale pink), flat cisterna (FC; green), light vesicle (yellow) and membranous sac (MS; pink) are depicted. (a) The MS in longitudinal views of the cytokinetic plane. (b) The MS in transversal views of the cytokinetic plane. Scale bars, 500 nm. (JPEG 22 kb)

High Resolution Image (TIFF 9604 kb)

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Nagasato, C., Kajimura, N., Terauchi, M. et al. Electron tomographic analysis of cytokinesis in the brown alga Silvetia babingtonii (Fucales, Phaeophyceae). Protoplasma 251, 1347–1357 (2014). https://doi.org/10.1007/s00709-014-0635-y

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