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Dynamic reorganization of the endomembrane system during spermatogenesis in Marchantia polymorpha

Journal of Plant Research volume 130, pages 433–441 (2017)Cite this article

Abstract

The processes involved in sexual reproduction have been diversified during plant evolution. Whereas charales, bryophytes, pteridophytes, and some gymnosperms utilize motile sperm as male gametes, in other gymnosperms and angiosperms the immotile sperm cells are delivered to the egg cells through elongated pollen tubes. During formation of the motile sperms, cells undergo a dynamic morphological transformation including drastic changes in shape and the generation of locomotor architecture. The molecular mechanism involved in this process remains mostly unknown. Membrane trafficking fulfills the exchange of various proteins and lipids among single membrane-bound organelles in eukaryotic cells, contributing to various biological functions. RAB GTPases and SNARE proteins are evolutionarily conserved key machineries of membrane trafficking mechanisms, which regulate tethering and fusion of the transport vesicles to target membranes. Our observation of fluorescently tagged plasma membrane-resident SNARE proteins demonstrated that these proteins relocalize to spherical structures during the late stages in spermiogenesis. Similar changes in subcellular localization were also observed for other fluorescently tagged SNARE proteins and a RAB GTPase, which acts on other organelles including the Golgi apparatus and endosomes. Notably, a vacuolar SNARE, MpVAMP71, was localized on the membrane of the spherical structures. Electron microscopic analysis revealed that there are many degradation-related structures such as multi-vesicular bodies, autophagosomes, and autophagic bodies containing organelles. Our results indicate that the cell-autonomous degradation pathway plays a crucial role in the removal of membrane components and the cytoplasm during spermiogenesis of Marchantia polymorpha. This process differs substantially from mammalian spermatogenesis in which phagocytic removal of excess cytoplasm involves neighboring cells.

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Acknowledgements

We thank Dr. Atsuko Era for sharing unpublished results. This work was supported by Grants-in-Aid for Scientific Research of the Ministry of Education, Culture, Sports, Science, and Technology of Japan and by a Grant-in-Aid for JSPS Fellows (N.M. and T.K.). This research was also supported by JST, PRESTO.

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Authors and Affiliations

  1. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan

    Naoki Minamino, Takehiko Kanazawa & Akihiko Nakano

  2. Division of Cellular Dynamics, National Institute for Basic Biology, Nishigonaka 38, Myodaiji, Okazaki, Aichi, 444-8585, Japan

    Naoki Minamino, Takehiko Kanazawa & Takashi Ueda

  3. Graduate School of Biostudies, Kyoto University, Kitashirakawa-oiwake-cho, Sakyo-ku, Kyoto, 606-8502, Japan

    Ryuichi Nishihama & Takayuki Kohchi

  4. Faculty of Biology-Oriented Science and Technology, Kindai University, Nishimitani, Kinokawa, Wakayama, 649-6493, Japan

    Katsuyuki T. Yamato

  5. Graduate School of Science, Kobe University, 1-1 Rokkodai, Nada-ku, Kobe, 657-8501, Japan

    Kimitsune Ishizaki

  6. Live Cell Super-Resolution Imaging Research Team, RIKEN Center for Advanced Photonics, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan

    Akihiko Nakano

  7. Japan Science and Technology Agency (JST), PRESTO, 4-1-8 Honcho Kawaguchi, Saitama, 332-0012, Japan

    Takashi Ueda

  8. Department of Basic Biology, SOKENDAI (Graduate University for Advanced Studies), Okazaki, Aichi, 444-8585, Japan

    Takashi Ueda

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  1. Naoki Minamino
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  2. Takehiko Kanazawa
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  3. Ryuichi Nishihama
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  4. Katsuyuki T. Yamato
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  5. Kimitsune Ishizaki
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  6. Takayuki Kohchi
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  7. Akihiko Nakano
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  8. Takashi Ueda
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Correspondence to Takashi Ueda.

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Minamino, N., Kanazawa, T., Nishihama, R. et al. Dynamic reorganization of the endomembrane system during spermatogenesis in Marchantia polymorpha . J Plant Res 130, 433–441 (2017). https://doi.org/10.1007/s10265-017-0909-5

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  • DOI: https://doi.org/10.1007/s10265-017-0909-5

Keywords

  • Marchantia polymorpha
  • Spermatogenesis
  • Endocytosis
  • Autophagy
  • Vacuole