How plants acquired the membrane trafficking system connecting inside and outside cells?

• Project/Area Number: 18H02470
• Research Category: Grant-in-Aid for Scientific Research (B)
• Allocation Type: Single-year Grants
• Section: 一般
• Review Section: Basic Section 44030:Plant molecular biology and physiology-related
• Research Institution: National Institute for Basic Biology
• Principal Investigator: Ueda Takashi 基礎生物学研究所, 細胞動態研究部門, 教授 (10311333)
• Project Period (FY): 2018-04-01 – 2021-03-31
• Project Status: Completed (Fiscal Year 2020)
• Budget Amount: ¥17,420,000 (Direct Cost: ¥13,400,000、Indirect Cost: ¥4,020,000); Fiscal Year 2020: ¥5,460,000 (Direct Cost: ¥4,200,000、Indirect Cost: ¥1,260,000); Fiscal Year 2019: ¥5,460,000 (Direct Cost: ¥4,200,000、Indirect Cost: ¥1,260,000); Fiscal Year 2018: ¥6,500,000 (Direct Cost: ¥5,000,000、Indirect Cost: ¥1,500,000)
• Keywords: エンドサイトーシス / エキソサイトーシス / クラスリン / ANTHドメイン / シロイヌナズナ / ゼニゴケ / RAB GTPase / エンドサイトーシス経路 / 分泌経路 / PICALM / 膜交通 / 多様化 / Rab GTPase / ANTH / exocyst / 細胞膜 / RAB / SNARE / 分泌

Outline of Final Research Achievements

Through functional analyses of endocytosis- and exocytosis-related molecules that have significantly diversified during land plant evolution, we attempted to elucidate the molecular mechanisms of membrane trafficking underpinning the plasma membrane function and reconstruct the evolutionary path of diversification of exocytic and endocytic trafficking. We found that the functions of the PICALM family, which act as clathrin adapters, have diversified during land plant evolution to play important roles in various developmental stages of plants, such as sexual reproduction and vegetative growth by being involved in endocytosis of distinct sets of proteins. We also found that RAB11 and RAB8, both of which are expected to act in the secretory pathway, may function by forming a cascade in a late step of secretion.

Academic Significance and Societal Importance of the Research Achievements

細胞の内側から外側へ，あるいは外側から内側へと物質を輸送する仕組みは，生命を維持するために欠かせないものです．この仕組みは進化の過程でそれぞれの生物ごとに変化し，洗練されてきました．この研究では，この進化の過程を植物を用いて明らかにすることで，現在の植物細胞内の物質輸送の仕組みがどのように出来上がってきたのかを明らかにしました．

Research Products

• [Int'l Joint Research] Heidelberg University/Max Planck Institute/Osnabruck University(ドイツ)
• [Int'l Joint Research] Universidad Nacional del Litoral(アルゼンチン)
• [Int'l Joint Research] Monash University/The University of Melbourne(オーストラリア)
• [Int'l Joint Research] Heidelberg University(ドイツ)
• [Journal Article] Identification of genes involved in <i>Meloidogyne incognita</i>-induced gall formation processes in <i>Arabidopsis thaliana</i> (2021)
  • Author(s): Suzuki Reira、Ueda Takashi、Wada Takuji、Ito Masaki、Ishida Takashi、Sawa Shinichiro
  • Journal Title: Plant Biotechnology Volume: 38 Issue: 1 Pages: 1-8
  • DOI: 10.5511/plantbiotechnology.20.0716a
  • NAID: 130008002844
  • ISSN: 1342-4580, 1347-6114
  • Year and Date: 2021-03-25
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Temperature-dependent fasciation mutants provide a link between mitochondrial RNA processing and lateral root morphogenesis (2021)
  • Author(s): Otsuka Kurataka、Mamiya Akihito、Konishi Mineko、Nozaki Mamoru、Kinoshita Atsuko、Tamaki Hiroaki、Arita Masaki、Saito Masato、Yamamoto Kayoko、Hachiya Takushi、Noguchi Ko、Ueda Takashi、Yagi Yusuke、Kobayashi Takehito、Nakamura Takahiro、Sato Yasushi、Hirayama Takashi、Sugiyama Munetaka
  • Journal Title: eLife Volume: 10
  • DOI: 10.7554/elife.61611
  • Peer Reviewed / Open Access
• [Journal Article] Cargo sorting zones in the trans-Golgi network visualized by super-resolution confocal live imaging microscopy in plants (2021)
  • Author(s): Shimizu Yutaro、Takagi Junpei、Ito Emi、Ito Yoko、Ebine Kazuo、Komatsu Yamato、Goto Yumi、Sato Mayuko、Toyooka Kiminori、Ueda Takashi、Kurokawa Kazuo、Uemura Tomohiro、Nakano Akihiko
  • Journal Title: Nature Communications Volume: 12 Issue: 1 Pages: 1901-1901
  • DOI: 10.1038/s41467-021-22267-0
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Oil Body Formation in Marchantia polymorpha Is Controlled by MpC1HDZ and Serves as a Defense against Arthropod Herbivores (2020)
  • Author(s): Romani F., Banic E., Florent S.N., Kanazawa T., Goodger J.Q.D., Mentink R.A., Dierschke T., Zachgo S., Ueda T., Bowman J.L., Tsiantis M., Moreno J.E.
  • Journal Title: Current Biology Volume: 30 Issue: 14 Pages: 2815-2828.e8
  • DOI: 10.1016/j.cub.2020.05.081
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Characterization of ancestral myosin XI from Marchantia polymorpha by heterologous expression in Arabidopsis thaliana (2020)
  • Author(s): Duan Zhongrui、Tanaka Misato、Kanazawa Takehiko、Haraguchi Takeshi、Takyu Akiko、Era Atsuko、Ueda Takashi、Ito Kohji、Tominaga Motoki
  • Journal Title: The Plant Journal Volume: 104 Issue: 2 Pages: 460-473
  • DOI: 10.1111/tpj.14937
  • Peer Reviewed
• [Journal Article] Longin R-SNARE is retrieved from the plasma membrane by ANTH domain-containing proteins in Arabidopsis (2020)
  • Author(s): Fujimoto Masaru、Ebine Kazuo、Nishimura Kohji、Tsutsumi Nobuhiro、Ueda Takashi
  • Journal Title: Proceedings of the National Academy of Sciences Volume: 117 Issue: 40 Pages: 25150-25158
  • DOI: 10.1073/pnas.2011152117
  • Peer Reviewed / Open Access
• [Journal Article] The Arabidopsis V-ATPase is localized to the TGN/EE via a seed plant-specific motif (2020)
  • Author(s): Lupanga U., Rohrich R., Askani J., Hilmer S., Kiefer C., Krebs M., Kanazawa T., Ueda T., Schumacher K.
  • Journal Title: eLife Volume: 9
  • DOI: 10.7554/elife.60568
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] The liverwort oil body is formed by redirection of the secretory pathway (2020)
  • Author(s): Kanazawa T., Morinaka H., Ebine K., Shimada T.L., Ishida S., Minamino N., Yamaguchi K., Shigenobu S., Kohchi T., Nakano A., Ueda T.
  • Journal Title: Nature Communications Volume: 11 Issue: 1 Pages: 6152-6152
  • DOI: 10.1038/s41467-020-19978-1
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Role of Autophagy in Male Reproductive Processes in Land Plants (2020)
  • Author(s): Norizuki Takuya、Minamino Naoki、Ueda Takashi
  • Journal Title: Frontiers in Plant Science Volume: 11 Pages: 756-756
  • DOI: 10.3389/fpls.2020.00756
  • Peer Reviewed / Open Access
• [Journal Article] Purification and Interaction Analysis of a Plant-Specific RAB5 Effector by In Vitro Pull-Down Assay (2020)
  • Author(s): Ito Emi、Choi Seung-won、Ueda Takashi
  • Journal Title: Methods in Molecular Biology Volume: 2177 Pages: 183-197
  • DOI: 10.1007/978-1-0716-0767-1_15
  • ISBN: 9781071607664, 9781071607671
  • Peer Reviewed
• [Journal Article] Deep Imaging Analysis in VISUAL Reveals the Role of YABBY Genes in Vascular Stem Cell Fate Determination (2020)
  • Author(s): Nurani Alif Meem、Ozawa Yasuko、Furuya Tomoyuki、Sakamoto Yuki、Ebine Kazuo、Matsunaga Sachihiro、Ueda Takashi、Fukuda Hiroo、Kondo Yuki
  • Journal Title: Plant and Cell Physiology Volume: 61 Issue: 2 Pages: 255-264
  • DOI: 10.1093/pcp/pcaa002
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Enrichment of Phosphatidylinositol 4,5-Bisphosphate in the Extra-Invasive Hyphal Membrane Promotes Colletotrichum Infection of Arabidopsis thaliana (2019)
  • Author(s): Shimada Takashi L、Betsuyaku Shigeyuki、Inada Noriko、Ebine Kazuo、Fujimoto Masaru、Uemura Tomohiro、Takano Yoshitaka、Fukuda Hiroo、Nakano Akihiko、Ueda Takashi
  • Journal Title: Plant and Cell Physiology Volume: 60 Issue: 7 Pages: 1514-1524
  • DOI: 10.1093/pcp/pcz058
  • Peer Reviewed
• [Journal Article] Marchantia polymorpha, a New Model Plant for Autophagy Studies (2019)
  • Author(s): Norizuki T., Kanazawa T., Minamino N., Tsukaya H., Ueda T.
  • Journal Title: Frontiers in Plant Science Volume: 10 Pages: 935-935
  • DOI: 10.3389/fpls.2019.00935
  • Peer Reviewed / Open Access
• [Journal Article] The RopGEF KARAPPO Is Essential for the Initiation of Vegetative Reproduction in Marchantia polymorpha (2019)
  • Author(s): Hiwatashi T., Goh H., Yasui Y., Koh L.Q., Takami H., Kajikawa M., Kirita H., Kanazawa T., Minamino N., Togawa T., Sato M., Wakazaki M., Yamaguchi K., Shigenobu S., Fukaki H., Mimura T., Toyooka K., Sawa S., Yamato K.T.,Ueda T., Urano D., Kohchi T., Ishizaki K.
  • Journal Title: Current Biology Volume: 29 Issue: 20 Pages: 3525-3531
  • DOI: 10.1016/j.cub.2019.08.071
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Protamines from liverwort are produced by posttranslational cleavage and C-terminal di-aminopropanelation of several male germ-specific H1 histones (2019)
  • Author(s): D'Ippolito, RA., Minamino, N, Rivera-Casas, C., Cheema, MS, Bai, DL., Kasinsky, HE., Shabanowitz, J., Eirin-Lopez, JM., Ueda, T., Hunt, DF., and Ausio, J.
  • Journal Title: J. Biol. Chem. Volume: 未定 Issue: 44 Pages: 16364-16373
  • DOI: 10.1074/jbc.ra119.010316
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] RAB GTPases and their effectors in plant endosomal transport (2019)
  • Author(s): 1)Minamino, N. and Ueda, T.
  • Journal Title: Curr. Opin. Plant Biol. Volume: 52 Pages: 61-68
  • DOI: 10.1016/j.pbi.2019.07.007
  • Peer Reviewed
• [Journal Article] A whole-cell electron tomography model of vacuole biogenesis in Arabidopsis root cells (2018)
  • Author(s): Cui Yong、Cao Wenhan、He Yilin、Zhao Qiong、Wakazaki Mayumi、Zhuang Xiaohong、Gao Jiayang、Zeng Yonglun、Gao Caiji、Ding Yu、Wong Hiu Yan、Wong Wing Shing、Lam Ham Karen、Wang Pengfei、Ueda Takashi、Rojas-Pierce Marcela、Toyooka Kiminori、Kang Byung-Ho、Jiang Liwen
  • Journal Title: Nature Plants Volume: 5 Issue: 1 Pages: 95-105
  • DOI: 10.1038/s41477-018-0328-1
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] A Golgi-Released Subpopulation of the Trans-Golgi Network Mediates Protein Secretion in Arabidopsis (2018)
  • Author(s): Uemura Tomohiro、Nakano Ryohei Thomas、Takagi Junpei、Wang Yiming、Kramer Katharina、Finkemeier Iris、Nakagami Hirofumi、Tsuda Kenichi、Ueda Takashi、Schulze-Lefert Paul、Nakano Akihiko
  • Journal Title: Plant Physiology Volume: 179 Issue: 2 Pages: 519-532
  • DOI: 10.1104/pp.18.01228
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] RAB GTPases in the Basal Land Plant Marchantia polymorpha (2018)
  • Author(s): Minamino Naoki、Kanazawa Takehiko、Era Atsuko、Ebine Kazuo、Nakano Akihiko、Ueda Takashi
  • Journal Title: Plant Cell Phys. Volume: in press Issue: 4 Pages: 850-861
  • DOI: 10.1093/pcp/pcy027
  • Peer Reviewed / Open Access
• [Journal Article] Distinct sets of tethering complexes, SNARE complexes, and Rab GTPases mediate membrane fusion at the vacuole in Arabidopsis (2018)
  • Author(s): Takemoto Kodai、Ebine Kazuo、Askani Jana Christin、Kruger Falco、Gonzalez Zaida Andres、Ito Emi、Goh Tatsuaki、Schumacher Karin、Nakano Akihiko、Ueda Takashi
  • Journal Title: Proc Natl Acad Sci USA. Volume: 115 Issue: 10
  • DOI: 10.1073/pnas.1717839115
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Integration of two RAB5 groups during endosomal transport in plants (2018)
  • Author(s): Ito, E., Ebine, K., Choi, S., Uemura, T., Nakano, A. and Ueda, T.
  • Journal Title: eLife Volume: 7
  • Peer Reviewed / Open Access
• [Journal Article] Involvement of S-type anion channels in disease resistance against an oomycete pathogen in Arabidopsis seedling (2018)
  • Author(s): Kurusu, T., Mitsuka, D., Yagi, C., Kitahata, N., Tsutsui, T., Ueda, T., Yamamoto, Y., Negi, J., Iba, K., Betsuyaku, S., Kuchitsu, K.
  • Journal Title: Commun. Integr. Biol. Volume: 11 Pages: 1-6
  • Peer Reviewed / Open Access
• [Journal Article] Transcriptional switch for programmed cell death in pith parenchyma of sorghum stems. (2018)
  • Author(s): Fujimoto M, Sazuka T, Oda Y, Kawahigashi H, Wu J, Takanashi H, Ohnishi T, Yoneda JI, Ishimori M, Kajiya-Kanegae H, Hibara KI, Ishizuna F, Ebine K, Ueda T, Tokunaga T, Iwata H, Matsumoto T, Kasuga S, Yonemaru JI, Tsutsumi N
  • Journal Title: Proceedings of the National Academy of Sciences of the United States of America Volume: 115 Issue: 37
  • DOI: 10.1073/pnas.1807501115
  • Peer Reviewed / Open Access
• [Journal Article] ANTH domain-containing proteins are required for the pollen tube plasma membrane integrity via recycling ANXUR kinases (2018)
  • Author(s): Muro Keita、Matsuura-Tokita Kumi、Tsukamoto Ryoko、Kanaoka Masahiro M.、Ebine Kazuo、Higashiyama Tetsuya、Nakano Akihiko、Ueda Takashi
  • Journal Title: Communications Biology Volume: 1 Issue: 1 Pages: 152-152
  • DOI: 10.1038/s42003-018-0158-8
  • Peer Reviewed / Open Access
• [Presentation] How Plants acquired new organelles -Lessons from Marchantia (2020)
  • Author(s): Takashi Ueda
  • Organizer: International Webinar Series: From Cellular dynamics to Morphology
  • Int'l Joint Research / Invited
• [Presentation] Organelle functions and membrane trafficking in plant cells (2019)
  • Author(s): Takashi Ueda
  • Organizer: EMBO practical course
  • Int'l Joint Research / Invited
• [Presentation] Adaptor proteins involved in clathrin-mediated endocytosis in plant cells (2018)
  • Author(s): Takashi Ueda
  • Organizer: CoB workshop “Cellular gateways: expanding the role of endocytosis in plant development”
  • Int'l Joint Research / Invited
• [Presentation] Roles and regulation of membrane traffic in spermatogenesis of Marchantia polymorpha (2018)
  • Author(s): Takashi Ueda
  • Organizer: EMBO workshop “New shores in land plant evolution”
  • Int'l Joint Research / Invited
• [Remarks]
  • URL: https://www.nibb.ac.jp/pressroom/news/2020/09/22.html
• [Remarks]
  • URL: https://www.nibb.ac.jp/en/pressroom/news/2020/12/01.html
• [Remarks]
  • URL: https://www.nibb.ac.jp/pressroom/news/2020/12/01.html