Evolutionarily unique mechanistic framework of clathrin-mediated endocytosis in plants

Abstract

In plants, clathrin mediated endocytosis (CME) represents the major route for cargo internalisation from the cell surface. It has been assumed to operate in an evolutionary conserved manner as in yeast and animals. Here we report characterisation of ultrastructure, dynamics and mechanisms of plant CME as allowed by our advancement in electron microscopy and quantitative live imaging techniques. Arabidopsis CME appears to follow the constant curvature model and the bona fide CME population generates vesicles of a predominantly hexagonal-basket type; larger and with faster kinetics than in other models. Contrary to the existing paradigm, actin is dispensable for CME events at the surface but plays a unique role in collecting endocytic vesicles, sorting of internalised cargos and directional endosome movement that itself actively promote CME events. Internalized vesicles display a strongly delayed and sequential uncoating. These unique features highlight the independent evolution of the plant CME mechanism during the autonomous rise of multicellularity in eukaryotes.

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Source data files have been provided for Figures 1, 2, 3, and 5

Article and author information

Author details

  1. Madhumitha Narasimhan

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  2. Alexander Johnson

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  3. Roshan Prizak

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  4. Walter Anton Kaufmann

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  5. Shutang Tan

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0471-8285
  6. Barbara Casillas-Pérez

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  7. Jiří Friml

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    For correspondence
    jiri.friml@ist.ac.at
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8302-7596

Funding

H2020 European Research Council (742985)

  • Madhumitha Narasimhan
  • Jiří Friml

Austrian Science Fund (I3630B25)

  • Alexander Johnson
  • Jiří Friml

European Molecular Biology Organization (ALTF 723-2015)

  • Shutang Tan

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. María Isabel Geli, Institut de Biología Molecular de Barcelona (IBMB), Spain

Publication history

  1. Received: September 20, 2019
  2. Accepted: January 22, 2020
  3. Accepted Manuscript published: January 23, 2020 (version 1)
  4. Version of Record published: February 11, 2020 (version 2)

Copyright

© 2020, Narasimhan et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Madhumitha Narasimhan
  2. Alexander Johnson
  3. Roshan Prizak
  4. Walter Anton Kaufmann
  5. Shutang Tan
  6. Barbara Casillas-Pérez
  7. Jiří Friml
(2020)
Evolutionarily unique mechanistic framework of clathrin-mediated endocytosis in plants
eLife 9:e52067.
https://doi.org/10.7554/eLife.52067
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