Evolution of the membrane trafficking system associated with acquisition and secondary loss of RAB GTPases and SNAREs

• Project/Area Number: 15H04382
• Research Category: Grant-in-Aid for Scientific Research (B)
• Allocation Type: Single-year Grants
• Section: 一般
• Research Field: Plant molecular biology/Plant physiology
• Research Institution: National Institute for Basic Biology (2016-2017); The University of Tokyo (2015)
• 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): 2015-04-01 – 2018-03-31
• Project Status: Completed (Fiscal Year 2017)
• Budget Amount: ¥17,940,000 (Direct Cost: ¥13,800,000、Indirect Cost: ¥4,140,000); Fiscal Year 2017: ¥5,590,000 (Direct Cost: ¥4,300,000、Indirect Cost: ¥1,290,000); Fiscal Year 2016: ¥5,590,000 (Direct Cost: ¥4,300,000、Indirect Cost: ¥1,290,000); Fiscal Year 2015: ¥6,760,000 (Direct Cost: ¥5,200,000、Indirect Cost: ¥1,560,000)
• Keywords: 膜交通 / 多様化 / 進化 / RAB GTPase / SNARE / Rab GTPase / 植物

Outline of Final Research Achievements

We performed functional analyses of RAB GTPases and SNARE proteins newly acquired or secondarily lost during plant evolution. We found that PUF2, an effector protein of plant-unique RAB GTPase ARA6, also interacts with canonical RAB5 in a competitive manner with ARA6 to integrate functions of the two groups of RAB GTPases. We also discovered that the plant-specific SNARE protein, VAMP727, mediates membrane fusion between endosomes and the vacuolar membrane in cooperation with RAB5 and the CORVET complex, while its homolog VAMP71 mediates membrane fusion between vacuoles with RAB7 and the HOPS complex. Furthermore, we unraveled that distinct groups of ANTH domain-containing proteins mediate endocytosis of distinctive cargo proteins including SNARE proteins and receptor-like kinases.

Research Products

• [Int'l Joint Research] Heidelberg University/Max Planck Institute(Germany)
• [Int'l Joint Research] ETH Zurich(Switzerland)
• [Int'l Joint Research] Monash University(オーストラリア)
• [Int'l Joint Research] University of Toronto(Canada)
• [Int'l Joint Research] Umea Plant Science Center(Sweden)
• [Int'l Joint Research] Gregor Mendel Institute(Austria)
• [Int'l Joint Research] Sainsbury Institute(United Kingdom)
• [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] 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] The Cellulose Synthases Are Cargo of the TPLATE Adaptor Complex (2018)
  • Author(s): Sanchez-Rodriguez Clara、Shi Yanyun、Kesten Christopher、Zhang Dongmei、Sancho-Andres Gloria、Ivakov Alexander、Lampugnani Edwin R.、Sklodowski Kamil、Fujimoto Masaru、Nakano Akihiko、Bacic Antony、Wallace Ian S.、Ueda Takashi、Van Damme Daniel、Zhou Yihua、Persson Staffan
  • Journal Title: Mol. Plant Volume: 11 Issue: 2 Pages: 346-349
  • DOI: 10.1016/j.molp.2017.11.012
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome. (2017)
  • Author(s): Bowman J, Kouchi T,..(106名）..Yokoyama R, ..(4名)
  • Journal Title: Cell Volume: 171 Issue: 2 Pages: 287-304
  • DOI: 10.1016/j.cell.2017.09.030
  • NAID: 120006353839
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] The GYF domain protein PSIG1 dampens the induction of cell death during plant-pathogen interactions (2017)
  • Author(s): Matsui Hidenori、Nomura Yuko、Egusa Mayumi、Hamada Takahiro、Hyon Gang-Su、Kaminaka Hironori、Watanabe Yuichiro、Ueda Takashi、Trujillo Marco、Shirasu Ken、Nakagami Hirofumi
  • Journal Title: PLOS Genet． Volume: 13 Issue: 10 Pages: 1-29
  • DOI: 10.1371/journal.pgen.1007037
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Triphosphate Tunnel Metalloenzyme Function in Senescence Highlights a Biological Diversification of This Protein Superfamily (2017)
  • Author(s): Ung Huoi、Karia Purva、Ebine Kazuo、Ueda Takashi、Yoshioka Keiko、Moeder Wolfgang
  • Journal Title: Plant Phys. Volume: 175 Issue: 1 Pages: 473-485
  • DOI: 10.1104/pp.17.00700
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Constitutive activation of plant-specific RAB5 GTPase confers increased resistance against adapted powdery mildew fungus (2017)
  • Author(s): Inada, N., Ebine, K., Ito, E., Nakano, A., and Ueda, T.
  • Journal Title: Plant Biotechnology Volume: 34 Issue: 2 Pages: 89-95
  • DOI: 10.5511/plantbiotechnology.17.0501a
  • NAID: 130006789286
  • ISSN: 1342-4580, 1347-6114
  • Peer Reviewed / Open Access
• [Journal Article] The trans-Golgi network and the Golgi stacks behave independently during regeneration after Brefeldin A treatment in tobacco BY-2 cells (2017)
  • Author(s): Ito, Y., Toyooka, K., Fujimoto, M., Ueda, T., Uemura, T. and Nakano A.
  • Journal Title: Plant Cell Phys. Volume: 印刷中 Issue: 4 Pages: 811-821
  • DOI: 10.1093/pcp/pcx028
  • Peer Reviewed / Open Access
• [Journal Article] Dynamic reorganization of the endomembrane system during spermatogenesis in Marchantia polymorpha (2017)
  • Author(s): Minamino, N., Kanazawa, T., Nishihama, R., Yamato, T.K., Ishizaki, K., Kohchi, T., Nakano, A. and Ueda, T.
  • Journal Title: J. Plant Res. Volume: 印刷中 Issue: 3 Pages: 433-441
  • DOI: 10.1007/s10265-017-0909-5
  • Peer Reviewed / Acknowledgement Compliant
• [Journal Article] Exocytic trafficking pathways in plants: why and how they are redirected (2017)
  • Author(s): Kanazawa Takehiko、Ueda Takashi
  • Journal Title: New Phytol. Volume: 215 Issue: 3 Pages: 952-957
  • DOI: 10.1111/nph.14613
  • Peer Reviewed / Open Access
• [Journal Article] MONENSIN SENSITIVITY 1 (MON1)/CALCIUM CAFFEINE ZINC SENSITIVITY 1 (CCZ1)-mediated Rab7 activation regulates tapetal programmed cell death and pollen development (2017)
  • Author(s): Cui, Y., Zhao, Q., Xie, HT., Wong, WS., Gao, C., Ding, Y., Tan, Y., Ueda, T., Zhang, Y. and Jiang, L.
  • Journal Title: Plant Physiol. Volume: 173 Issue: 1 Pages: 206-218
  • DOI: 10.1104/pp.16.00988
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases (2016)
  • Author(s): Mbengue, M., Bourdais, G., Gervasi, F., Beck, M., Zhou, J., Spallek, T., Bartels, S., Boller, T., Ueda, T., Kuhn, H. and Robatzek, S.
  • Journal Title: Proc Natl Acad Sci USA. Volume: 113 Issue: 39 Pages: 11034-11039
  • DOI: 10.1073/pnas.1606004113
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] DRP1-dependent Endocytosis Is Essential for Polar Localization and Boron-induced Degradation of the Borate Transporter BOR1 in Arabidopsis thaliana (2016)
  • Author(s): Yoshinari, A., Fujimoto, M., Ueda, T., Inada, N., Naito, S. and Takano, J.
  • Journal Title: Plant Cell Phys. Volume: 57 Issue: 9 Pages: 1985-2000
  • DOI: 10.1093/pcp/pcw121
  • Peer Reviewed
• [Journal Article] ENDOSOMAL RAB EFFECTOR WITH PX-DOMAIN, an Interacting Partner of RAB5 GTPases, Regulates Membrane Trafficking to Protein Storage Vacuoles in Arabidopsis (2016)
  • Author(s): Sakurai, H., Inoue, T., Nakano, A. and Ueda, T.
  • Journal Title: Plant Cell Volume: 26 Issue: 6 Pages: 1490-0503
  • DOI: 10.1105/tpc.16.00326
  • Peer Reviewed / Acknowledgement Compliant
• [Journal Article] Modulation of plant RAB GTPase-mediated membrane trafficking pathway at the interface between plants and obligate biotrophic pathogens. (2016)
  • Author(s): Inada, N., Betsuyaku, S., Shimada, T., Ebine, K., Ito, E., Kutsuna, N., Hasezawa, S., Takano, Y., Fukuda, H., Nakano, A., & Ueda, T.
  • Journal Title: Plant Cell Physiol. Volume: 57 Issue: 9 Pages: 1854-1864
  • DOI: 10.1093/pcp/pcw107
  • Peer Reviewed / Open Access
• [Journal Article] AtNHX5 and AtNHX6 Are Required for the Subcellular Localization of the SNARE Complex That Mediates the Trafficking of Seed Storage Proteins in Arabidopsis. (2016)
  • Author(s): Wu X, Ebine K, Ueda T, Qiu QS.
  • Journal Title: PLoS One. Volume: 11 Issue: 3 Pages: e0151658-e0151658
  • DOI: 10.1371/journal.pone.0151658
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Accumulation of fluorescent proteins derived from a trans-Golgi cisternal membrane marker and paramural bodies in interdigitated apoplastic space in Arabidopsis leaf epidermis (2016)
  • Author(s): Akita, K., Kobayashi, M., Sato, M., Kutsuna, N., Ueda, T., Toyooka, K., Nagata, N., Hasezawa, S., and Higaki, T.
  • Journal Title: Protoplasma Volume: in press Issue: 1 Pages: 367-377
  • DOI: 10.1007/s00709-016-0955-1
  • Peer Reviewed / Open Access
• [Journal Article] Distribution of RAB5-positive multivesicular endosomes and the <i>trans</i>-Golgi network in root meristematic cells of <i>Arabidopsis thaliana</i> (2016)
  • Author(s): Ito, E., Uemura, T., Ueda, T. (corresponding author), and Nakano, A.
  • Journal Title: Plant Biotechnology Volume: 33 Issue: 4 Pages: 281-286
  • DOI: 10.5511/plantbiotechnology.16.0218a
  • NAID: 130005281074
  • ISSN: 1342-4580, 1347-6114
  • Peer Reviewed / Acknowledgement Compliant
• [Journal Article] Functional analyses of the plant-specific C-terminal region of VPS9a: the activating factor for RAB5 in Arabidopsis thaliana (2016)
  • Author(s): Sunada, M., Goh, T., Ueda, T. (corresponding author) and Nakano, A.
  • Journal Title: J. Plant Res. Volume: 129 Issue: 1 Pages: 93-102
  • DOI: 10.1007/s10265-015-0760-5
  • NAID: 40020697785
  • Peer Reviewed / Acknowledgement Compliant
• [Journal Article] SNARE Molecules in Marchantia polymorpha: Unique and Conserved Features of the Membrane Fusion Machinery. (2016)
  • Author(s): Kanazawa, T., Era, A., Minamino, N., Shikano, Y., Fujimoto, M., Uemura, T., Nishihama, R., Yamato, KT., Ishizaki, K., Nishiyama, T., Kohchi, T., Nakano, A., Ueda, T.
  • Journal Title: Plant Cell Physiol. Volume: 57 Issue: 2 Pages: 307-24
  • DOI: 10.1093/pcp/pcv076
  • Peer Reviewed / Open Access
• [Journal Article] The Naming of Names: Guidelines for Gene Nomenclature in Marchantia (2016)
  • Author(s): Bowman, J., Araki, T., Arteaga-Vazquez, M., Berger, F., Dolan, L., Haseloff, J., Ishizaki, K., Kyozuka, J., Lin, S.S., Nagasaki, H., Nakagami, H., Nakajima, K., Nakamura, Y., Ohashi-Ito, K., Sawa, S., Shimamura, M., Solano, R., Tsukaya, H., Ueda, T., Watanabe, Y., Yamato, K.T., Zachgo, S., and Kohchi, T.
  • Journal Title: Plnat cell Physiology Volume: 57 Issue: 2 Pages: 257-261
  • DOI: 10.1093/pcp/pcv193
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Anthocyanin Vacuolar Inclusions Form by a Microautophagy Mechanism (2015)
  • Author(s): Chanoca, A., Kovinich, N., Burkel, B., Stecha, S., Bohorquez-Restrepo, A., Ueda, T., Eliceiri, KW., Grotewold, E. and Otegui, MS.
  • Journal Title: Plant Cell Volume: 27 Issue: 9 Pages: 2545-2559
  • DOI: 10.1105/tpc.15.00589
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Guanine nucleotide exchange factor 2 for Rab5 proteins coordinated with GLUP6/GEF regulates the intracellular transport of the proglutelin from the Golgi apparatus to the protein storage vacuole in rice endosperm (2015)
  • Author(s): Wen, L., Fukuda, M., Sunada, M., Ishino, S., Ishino, Y., Okita, W.T., Ogawa, M., Ueda, T. and Kumamaru, T.
  • Journal Title: J. Exp. Bot. Volume: 66 Issue: 20 Pages: 6137-6147
  • DOI: 10.1093/jxb/erv325
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Roles of membrane trafficking in plant cell wall dynamics (2015)
  • Author(s): Ebine, K., and Ueda, T.
  • Journal Title: Front. Plant Sci. Volume: - Pages: 878-878
  • DOI: 10.3389/fpls.2015.00878
  • Peer Reviewed / Open Access / Acknowledgement Compliant
• [Journal Article] 細胞壁の構築・維持と膜交通システム (2015)
  • Author(s): 海老根一生，上田貴志
  • Journal Title: 植物の生長調節 Volume: 50 Pages: 43-49
• [Presentation] ゼニゴケ精子形成・機能に関わる膜交通システムの解析 (2017)
  • Author(s): 南野尚紀, 金澤建彦，法月卓也，西浜竜一，大和勝幸，石崎公庸，河内孝之，中野明彦，上田貴志
  • Organizer: 第58回日本植物生理学会年会
  • Place of Presentation: 鹿児島大学（鹿児島県，鹿児島市）
  • Year and Date: 2017-03-18
• [Presentation] ゼニゴケにおけるオートファジーの解析 (2017)
  • Author(s): 法月卓也, 金澤建彦，南野尚紀，西浜竜一，河内孝之，中野明彦，上田貴志
  • Organizer: 第58回日本植物生理学会年会
  • Place of Presentation: 鹿児島大学（鹿児島県，鹿児島市）
  • Year and Date: 2017-03-18
• [Presentation] HOPS/CORVET complexes in vacuolar trafficking pathways of A. thaliana (2017)
  • Author(s): Kodai Takemoto, Kazuo Ebine, Tatsuaki Goh, Jun Ito, Akihiko Nakano, Takashi Ueda
  • Organizer: 第58回日本植物生理学会年会
  • Place of Presentation: 鹿児島大学（鹿児島県，鹿児島市）
  • Year and Date: 2017-03-18
• [Presentation] 植物特異的オルガネラの獲得に伴う膜交通経路の再配向 (2017)
  • Author(s): 金澤建彦, 森中初音, 海老根一生, 法月拓也, 南野尚紀, 西浜竜一, 河内孝之, 中野明彦, 上田貴志
  • Organizer: 第58回日本植物生理学会年会
  • Place of Presentation: 鹿児島大学（鹿児島県，鹿児島市）
  • Year and Date: 2017-03-18
• [Presentation] Diversification of membrane trafficking pathways during land plant evolution (2017)
  • Author(s): 上田貴志
  • Organizer: 第58回植物生理学会年会
  • Place of Presentation: 鹿児島大学（鹿児島県，鹿児島市）
  • Year and Date: 2017-03-17
• [Presentation] Molecular mechanisms of vacuolar membrane fusion regulated by SNARE proteins in plant cells (2017)
  • Author(s): Kazuo Ebine, Kodai Takemoto, Chieko Saito, Tomohiro Uemura, Akihiko Nakano, and Takashi Ueda
  • Organizer: 第58回日本植物生理学会年会
  • Place of Presentation: 鹿児島大学（鹿児島県，鹿児島市）
  • Year and Date: 2017-03-17
• [Presentation] ホスファチジルイノシトールリン酸を介した炭疽病菌感染機構の解明 (2017)
  • Author(s): 島田 貴士，高野 義孝，別役 重之，中野 明彦，上田 貴志
  • Organizer: 第58回日本植物生理学会年会
  • Place of Presentation: 鹿児島大学（鹿児島県，鹿児島市）
  • Year and Date: 2017-03-17
• [Presentation] Diversification of membrane trafficking pathways during land plant evolution unraveled with Marchantia polymorpha (2017)
  • Author(s): Ueda Takashi
  • Organizer: The 65th NIBB conference Renaissance of Marchantia polymorpha -the genome and beyond-
  • Int'l Joint Research / Invited
• [Presentation] Evolution of plant membrane trafficking system driven by diversification of RAB and SNARE protreins (2017)
  • Author(s): Ueda Takashi
  • Organizer: 4th AoE Symposium on Organelle Biogenesis and Function
  • Int'l Joint Research / Invited
• [Presentation] Diversification of membrane trafficking pathways during land plant evolution (2017)
  • Author(s): Ueda Takashi
  • Organizer: Taiwan-Japan Plant Biology 2017
  • Int'l Joint Research / Invited
• [Presentation] Diversification of membrane trafficking pathways during land plant evolution (2017)
  • Author(s): Ueda Takashi
  • Organizer: SEB Gothenburg 2017
  • Int'l Joint Research / Invited
• [Presentation] 植物細胞のダイナミクスを支える膜交通 (2016)
  • Author(s): 上田貴志
  • Organizer: 第39回日本分子生物学会年会
  • Place of Presentation: パシフィコ横浜（神奈川県，横浜市）
  • Year and Date: 2016-12-02
• [Presentation] 陸上植物固有のR-SNAREに存在する挿入配列の機能とその起源 (2016)
  • Author(s): 藤本優，海老根一生，石崎公庸，大和勝幸，深尾陽一朗，植村知博，丸山桃子，井坂奈々子，河内孝之，中野明彦，上田貴志
  • Organizer: 第39回日本分子生物学会年会
  • Place of Presentation: パシフィコ横浜（神奈川県，横浜市）
  • Year and Date: 2016-12-01
  • Invited
• [Presentation] 細胞内交通システムの研究から探る植物のチカラ (2016)
  • Author(s): 上田貴志
  • Organizer: 大学共同利用機関シンポジウム2016
  • Place of Presentation: 秋葉原UDX（東京都，千代田区）
  • Year and Date: 2016-11-27
  • Invited
• [Presentation] ゼニゴケで見えてきた細胞骨格と膜交通の深い仲 (2016)
  • Author(s): 上田貴志
  • Organizer: 細胞骨格研究会－PlantCytoskeleton2016－
  • Place of Presentation: 東京大学（東京都，目黒区）
  • Year and Date: 2016-11-25
  • Invited
• [Presentation] ステロール恒常性の制御を行う新規小胞体タンパク質 (2016)
  • Author(s): 島田貴士，嶋田知生，岡咲洋三，東浩司，斉藤和季，中野明彦，上田貴志，高野義孝，西村いくこ
  • Organizer: 第29回植物脂質シンポジウム
  • Place of Presentation: 大阪大学（大阪府，豊中市）
  • Year and Date: 2016-11-25
• [Presentation] Twins or Convergence? ~two plant-unique cellular structures acquired during evolution~ (2016)
  • Author(s): Takashi Ueda
  • Organizer: International Symposium “Front Lines of Plant Cell Wall Research and Beyond”
  • Place of Presentation: KKRホテル熱海（静岡県，熱海市）
  • Year and Date: 2016-10-05
  • Int'l Joint Research / Invited
• [Presentation] 液胞膜のSNARE複合体制御メカニズムの解析 (2016)
  • Author(s): 海老根一生, 齊藤知恵子, 植村知博, 中野明彦, 上田貴志
  • Organizer: 第80回日本植物学会大会
  • Place of Presentation: 沖縄コンベンションセンター（沖縄県，宜野湾市）
  • Year and Date: 2016-09-16
• [Presentation] Diversification of membrane trafficking pathways ~lessons from the liverwort~ (2016)
  • Author(s): Takashi Ueda
  • Organizer: EMBO workshop “New model systems for early land plant evolution”
  • Place of Presentation: Vienna, Austria
  • Year and Date: 2016-06-22
  • Int'l Joint Research / Invited
• [Presentation] Membrane trafficking system plays important roles in sperm functions of Marchantia polymorpha (2016)
  • Author(s): Naoki Minamino, Takehiko Kanazawa, Atsuko Era, Ryuichi Nishihama, Katsuyuki T. Yamato, Kimitsune Ishizaki, Takayuki Kohchi, Akihiko Nakano, Takashi Ueda
  • Organizer: EMBO workshop “New model systems for early land plant evolution”
  • Place of Presentation: Vienna, Austria
  • Year and Date: 2016-06-22
  • Int'l Joint Research
• [Presentation] Cell type-specific reorientation of a trafficking pathway led to acquisition of new organelles during land plant evolution (2016)
  • Author(s): Takehiko Kanazawa, Hatsune Morinaka, Takuya Norizuki, Atsuko Era, Naoki Minamino, Yu Shikano, Masaru Fujimoto, Tomohiro Uemura, Ryuichi Nishihama, Katsuyuki T. Yamato, Kimitsune Ishizaki, Tomoaki Nishiyama, Takayuki Kohchi, Akihiko Nakano, Takashi Ueda
  • Organizer: EMBO workshop “New model systems for early land plant evolution”
  • Place of Presentation: Vienna, Austria
  • Year and Date: 2016-06-22
  • Int'l Joint Research
• [Presentation] Diversification of membrane trafficking pathways during land plant evolution. (2016)
  • Author(s): Takashi Ueda
  • Organizer: 1st CRC 1101 symposium, Molecular Encoding of Specificity in Plant Processes
  • Place of Presentation: Tuebingen, Germany
  • Year and Date: 2016-04-05
  • Int'l Joint Research / Invited
• [Book] DOJIN BIOSCIENCEシリーズ メンブレントラフィック (2016)
  • Author(s): 上田貴志（他29名），福田光則，吉森保編
  • Total Pages: 262
  • Publisher: 化学同人
• [Book] 植物細胞壁実験法 (2016)
  • Author(s): 伊藤瑛海，藤本優，石井みどり，上田貴志（分担執筆）
  • Total Pages: 403
  • Publisher: 弘前大学出版会
• [Remarks] 研究室web page
  • URL: http://www.nibb.ac.jp/cellular/