Dynamic reorganization of the endomembrane system during spermatogenesis in Marchantia polymorpha.
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.
Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan.|Division of Cellular Dynamics, National Institute for Basic Biology, Nishigonaka 38, Myodaiji, Okazaki, Aichi, 444-8585, Japan.
Naoki
N
Minamino
Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan.|Division of Cellular Dynamics, National Institute for Basic Biology, Nishigonaka 38, Myodaiji, Okazaki, Aichi, 444-8585, Japan.
Takehiko
T
Kanazawa
Graduate School of Biostudies, Kyoto University, Kitashirakawa-oiwake-cho, Sakyo-ku, Kyoto, 606-8502, Japan.
Ryuichi
R
Nishihama
Faculty of Biology-Oriented Science and Technology, Kindai University, Nishimitani, Kinokawa, Wakayama, 649-6493, Japan.
Katsuyuki T
KT
Yamato
Graduate School of Science, Kobe University, 1-1 Rokkodai, Nada-ku, Kobe, 657-8501, Japan.
Kimitsune
K
Ishizaki
Graduate School of Biostudies, Kyoto University, Kitashirakawa-oiwake-cho, Sakyo-ku, Kyoto, 606-8502, Japan.
Takayuki
T
Kohchi
Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan.|Live Cell Super-Resolution Imaging Research Team, RIKEN Center for Advanced Photonics, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan.
Akihiko
A
Nakano
Division of Cellular Dynamics, National Institute for Basic Biology, Nishigonaka 38, Myodaiji, Okazaki, Aichi, 444-8585, Japan. tueda@nibb.ac.jp.|Japan Science and Technology Agency (JST), PRESTO, 4-1-8 Honcho Kawaguchi, Saitama, 332-0012, Japan. tueda@nibb.ac.jp.|Department of Basic Biology, SOKENDAI (Graduate University for Advanced Studies), Okazaki, Aichi, 444-8585, Japan. tueda@nibb.ac.jp.
Takashi
T
Ueda
D000071182:Autophagosomes / Q000378:metabolism / Q000502:physiology / Q000648:ultrastructure; D001343:Autophagy / Q000502:physiology; D002462:Cell Membrane / Q000378:metabolism / Q000648:ultrastructure; D004705:Endocytosis / Q000502:physiology; D011992:Endosomes / Q000378:metabolism / Q000502:physiology; D006056:Golgi Apparatus / Q000378:metabolism / Q000502:physiology / Q000648:ultrastructure; D047008:Marchantia / Q000235:genetics / Q000378:metabolism* / Q000502:physiology* / Q000648:ultrastructure; D008561:Membrane Fusion; D008565:Membrane Proteins / Q000378:metabolism; D008855:Microscopy, Electron, Scanning; D015388:Organelles / Q000502:physiology / Q000648:ultrastructure; D010940:Plant Proteins / Q000378:metabolism*; D021381:Protein Transport / Q000502:physiology; D012098:Reproduction / Q000502:physiology*; D050600:SNARE Proteins / Q000378:metabolism; D013091:Spermatogenesis / Q000502:physiology*; D014617:Vacuoles / Q000378:metabolism / Q000648:ultrastructure; D020691:rab GTP-Binding Proteins / Q000378:metabolism
D008565:Membrane Proteins; D010940:Plant Proteins; D050600:SNARE Proteins; D020691:rab GTP-Binding Proteins
Autophagy; Endocytosis; Marchantia polymorpha; Spermatogenesis; Vacuole