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A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6

Nature Cell Biology volume 13, pages 853859 (2011) | Download Citation

Abstract

Endosomal trafficking plays an integral role in various eukaryotic cell activities and serves as a basis for higher-order functions in multicellular organisms. An understanding of the importance of endosomal trafficking in plants is rapidly developing1,2, but its molecular mechanism is mostly unknown. Several key regulators of endosomal trafficking, including RAB5, which regulates diverse endocytic events in animal cells3,4, are highly conserved. However, the identification of lineage-specific regulators in eukaryotes indicates that endosomal trafficking is diversified according to distinct body plans and lifestyles. In addition to orthologues of metazoan RAB5, land plants possess a unique RAB5 molecule, which is one of the most prominent features of plant RAB GTPase organization5,6. Plants have also evolved a unique repertoire of SNAREs, the most distinctive of which are diverse VAMP7-related longins, including plant-unique VAMP72 derivatives7. Here, we demonstrate that a plant-unique RAB5 protein, ARA6, acts in an endosomal trafficking pathway in Arabidopsis thaliana. ARA6 modulates the assembly of a distinct SNARE complex from conventional RAB5, and has a functional role in the salinity stress response. Our results indicate that plants possess a unique endosomal trafficking network and provide the first indication of a functional link between a specific RAB and a specific SNARE complex in plants.

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Acknowledgements

We would like to thank T. Fujiwara, S. Utsumi, I. Hara-Nishimura, Y. Wada, J. Takano and M. T. Morita for sharing materials; E. Furuyama for technical support; and the SALK Institute, Max Planck Institute and ABRC for providing A. thaliana mutants. Sequence data for Selagninella moellendorffii and Volvox carterii were generated by the US Department of Energy Joint Genome Institute (http://www.jgi.doe.gov/). This work was supported by Grants-in-Aid for Scientific Research and the Targeted Proteins Research Program (TPRP) from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and Grant-in-Aid for JSPS Fellows (K.E., 195010).

Author information

Author notes

    • Tatsuaki Goh

    Present address: Department of Biology, Graduate School of Science, Kobe University, Kobe 657-8501, Japan

Affiliations

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

    • Kazuo Ebine
    • , Masaru Fujimoto
    • , Yusuke Okatani
    • , Tatsuaki Goh
    • , Emi Ito
    • , Tomoko Dainobu
    • , Tomohiro Uemura
    • , Akihiko Nakano
    •  & Takashi Ueda
  2. Advanced Science Research Center, Kanazawa University, 13-1 Takara-machi, Kanazawa, Ishikawa 920-0934, Japan

    • Tomoaki Nishiyama
  3. Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, 1-5, Shimogamo-nakaragi-cho, Sakyo-ku, Kyoto, Kyoto 606-8522, Japan

    • Aiko Nishitani
    •  & Masa H. Sato
  4. Department of Agriculture and Ecology, Faculty of Life Sciences, University of Copenhagen Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark

    • Hans Thordal-Christensen
  5. Laboratory of Plant Molecular Genetics, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan

    • Nobuhiro Tsutsumi
  6. Molecular Membrane Biology Laboratory, RIKEN Advanced Science Institute, Wako, Saitama 351-0198, Japan

    • Akihiko Nakano

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Contributions

T. Ueda designed the study; K.E. carried out the main parts of the genetic, biochemical and confocal microscopy experiments; M.F. and N.T. conducted TIRFM; T.G. carried out the experiments presented in Fig. 2c; T.N. carried out the phylogenetic analysis; Y.O., T.D., E.I., A. Nishitani, M.H.S. and T. Uemura constructed the transgenic plants used in this study; H.T-C. prepared the anti-SYP121 antibody; and A. Nakano and T. Ueda supervised the study.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Takashi Ueda.

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DOI

https://doi.org/10.1038/ncb2270

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