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Cleavage, incomplete inversion, and cytoplasmic bridges in Gonium pectorale (Volvocales, Chlorophyta)

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Abstract

Multicellularity arose several times in evolution of eukaryotes. The volvocine algae have full range of colonial organization from unicellular to colonies, and thus these algae are well-known models for examining the evolution and mechanisms of multicellularity. Gonium pectorale is a multicellular species of Volvocales and is thought to be one of the first small colonial organisms among the volvocine algae. In these algae, a cytoplasmic bridge is one of the key traits that arose during the evolution of multicellularity. Here, we observed the inversion process and the cytoplasmic bridges in G. pectorale using time-lapse, fluorescence, and electron microscopy. The cytoplasmic bridges were located in the middle region of the cell in 2-, 4-, 8-, and 16-celled stages and in inversion stages. However, there were no cytoplasmic bridges in the mature adult stage. Cytoplasmic bridges and cortical microtubules in G. pectorale suggest that a mechanism of kinesin-microtubule machinery similar to that in other volvocine algae is responsible for inversion in this species.

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Acknowledgments

We are grateful to Drs Ken-ichiro Ishida and Shinichi Miyamura (University of Tsukuba) for valuable advice during this research.

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Authors and Affiliations

  1. Takezono High School, 3-9-1 Takezono, Tsukuba, Ibaraki, 305-0032, Japan

    Hitoshi Iida

  2. Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba, 277-8562, Japan

    Shuhei Ota

  3. Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki, 305-8572, Japan

    Hitoshi Iida, Shuhei Ota & Isao Inouye

Authors
  1. Hitoshi Iida
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  2. Shuhei Ota
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  3. Isao Inouye
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Correspondence to Hitoshi Iida.

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10265_2013_553_MOESM1_ESM.avi

Supplementary Figure S1. Microscopic time-lapse video of inversion in G. pectorale: Embryogenesis from 4-celled embryo to mature 8-celled colonies. (AVI 2179 kb)

10265_2013_553_MOESM2_ESM.tif

Supplementary Figure S2. a Merged image of DIC, microtubules (green), and EtBr-stained nuclei (red) corresponding to Fig. 5d-f. b, c Microtubules of the posterior region of the embryo are shown along the z-axis. Note that few cortical microtubules are localized in the posterior region of each cell. (TIFF 953 kb)

10265_2013_553_MOESM3_ESM.tif

Supplementary Figure S3. Simplified schematic tree of the volvocine algae based on the phylogenetic analysis of Herron and Michod (2008). Black branches indicate multicellular species. Arrowhead indicates acquisition of cytoplasmic bridges in embryos. Double arrowhead indicates acquisition of complete inversion. Note that the genus Gonium is a member of the basal clade within Volvocales and incomplete inversion arose independently in the Gonium lineage. (TIFF 345 kb)

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Iida, H., Ota, S. & Inouye, I. Cleavage, incomplete inversion, and cytoplasmic bridges in Gonium pectorale (Volvocales, Chlorophyta). J Plant Res 126, 699–707 (2013). https://doi.org/10.1007/s10265-013-0553-7

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