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Cell Struct Funct
2024 Oct 03; doi: 10.1247/csf.24055.
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Cell-wide arrangement of Golgi/RE units depends on the microtubule organization.
Tago T
,
Fujii S
,
Sasaki S
,
Shirae-Kurabayashi M
,
Sakamoto N
,
Yamamoto T
,
Maeda M
,
Ueki T
,
Satoh T
,
Satoh AK
.
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We have previously shown that Golgi stacks and recycling endosomes (REs) exist as Golgi/RE units in sea urchin embryos. In this study, we showed that Golgi/RE units were scattered throughout the cytoplasm at early developmental stages but gathered to form a "Golgi ring" surrounding the centric REs at the blastula stage. This change in the cell-wide arrangement of Golgi/RE units coincided with a dramatic change in microtubule organization from a randomly oriented cortical pattern to radial arrays under the apical plasma membrane. A single gigantic Golgi apparatus surrounding centric RE is clearly associated with the center of the radial microtubule arrays. Furthermore, we found that in some animal species belonging to different clades, Golgi stacks lack lateral connections but are likely centralized by microtubule motors. These results suggest that Golgi centralization depends on the organization of the microtubule array in addition to the lateral linking between Golgi stacks. Key words: Golgi stack, recycling endosome, Golgi-ribbon, microtubule, cilium, sea urchin, ascidian.
Fig. 1. Cell-wide distribution of Golgi/REs in late-blastula-stage sea urchin embryos(A) Cis-Golgi cisternae, trans-Golgi cisternae, and RE at the late blastula stage of the sea urchin Hemicentrotus pulcherrimus visualized using the TagBFP2::Syx5 (blue), GalT::EGFP (green), and tdTomato::Vamp3 (red) after mRNA injections into fertilized oocytes. (B) Trans-Golgi cisternae and RE at the late blastula stage of the sea urchin H. pulcherrimus visualized using GalT::EGFP (green) and tdTomato::Rab11 (magenta) after mRNA injections into fertilized oocytes. (C–G) Electron micrograph of cells at the late blastula stage of the sea urchin Heliocidaris crassispina. Arrows in C indicate gigantic Golgi apparatus. D–G are higher magnification images of the Golgi apparatus in other sections. Arrows indicate electron-dense materials. Scale bars: 5 μm (A left), 1 μm (A right, B), 2 μm (C), 500 nm (D, E), and 1 μm (F, G).
Fig. 2. Cell-wide distribution of Golgi/REs in Ciona robusta embryos at tailbud stage(A) Trans-Golgi cisternae and RE of tailbud-staged ascidian, visualized using GalT::EGFP (green) and tdTomato::Vamp3 (magenta) after mRNA injections into fertilized oocytes. (B) Trans-Golgi cisternae and RE of tailbud stage ascidian, visualized using GalT::EGFP (green) and tdTomato::Rab11 (magenta) after mRNA injections into fertilized oocytes. (C–F) Electron micrograph of cells in of tailbud stage ascidian. Arrows in C indicate gigantic Golgi apparatus. D–F are higher magnification images of the Golgi apparatus in other sections. The arrow indicates the centriole. Scale bars: 5 μm (A left), 2 μm (A right, B), 2 μm (C), and 500 nm (D–F).
Fig. 3. Formation of a giant Golgi apparatus under the center of the microtubule organizing center at late blastula stage(A–D) Projection images of 43 (A), 31 (B) or 34 (C, D) sections with 0.3-μm interval in embryo cells of the sea urchin H. pulcherrimu. Trans-Golgi cisternae and microtubules were visualized using GalT::EGFP (magenta) after the mRNA was injected into fertilized oocytes. The samples were immunostained with anti-α-tubulin antibody (green). (A) Preblastula, (B, C) late blastula, and (D) intermediate stages. Arrows indicate MTOC. (E, F) Trans-Golgi cisternae, RE, and microtubules at the late blastula stage of the sea urchin H. pulcherrimus visualized using GalT::EGFP (green) and tdTomato::Vamp3 (red) after their mRNA was injected into fertilized oocytes. The samples were immunostained with anti-α-tubulin antibody (blue) at the late blastula stage. Arrows indicate REs on microtubules. Left and right are the projection images of 15 and 26 z-sections at 0.3-μm intervals, respectively. (G) 30-nm thick serial sections of the Golgi apparatus in a cell of the gastrula-stage sea urchin H. crassispina, observed by scanning electron microscopy. (H) Electron micrograph showing projections of the Golgi apparatus (yellow), cilia(blue), basal body (blue), and striated rootlet (red) made from the serial sections in (G). (I) Models for the cell-wide arrangement of Golgi/RE units in a cell at the gastrula stage of the sea urchin. Golgi stacks in green, REs in Red, microtubules and basal body in blue. Scale bars: 5 μm (A–F), and 1 μm (G, H).
Fig. 4. Schematic of animal evolution in metazoansThe schematic represents the phylogenetic tree of metazoans, adapted from Adoutte et al. (Adoutte et al., 2000) and Ueki et al. (Ueki et al., 2019). The phyla to which the animals used in the experiments belong are highlighted with red rectangles. Sea urchins H. pulcherrimus and H. crassispina belong to echinoderms, the ascidian C. robusta belongs to tunicates, the marine acoel worm P. naikaiensis belongs to xenacoelomorphs, and the mollusk A. esculentum belongs to mollusks.
Fig. 5. Golgi stacks clustered near centrosomes in Praesagittifera naikaiensis and Acanthosepion esculentum(A–C) An electron micrograph of a cell in the xenacoelomorph P. naikaiensis. B is magnified images of clustered Golgi stacks in a square in A. C is the clustered Golgi stacks in another specimen. (D–F) Electron micrograph of a cell in the embryo of the mollusk A. esculentum. E is magnified images of clustered Golgi stacks in a square in D. F is the clustered Golgi stacks in another specimen. The arrow indicates the centriole. (G, H) 90-nm thick serial sections of clustered Golgi stacks in an embryonic cell in the mollusk A. esculentum observed by scanning electron microscopy. H is magnified images of G. The arrows indicate the centriole. Scale bars: 2 μm (A), 500 nm (B, C), 2 μm (D), 1 μm (E), 500 nm (F), 5 μm (G), and 1 μm (H).
