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The TPLATE complex mediates membrane bending during plant clathrin–mediated endocytosis

Alexander Johnson, Dana A. Dahhan, Nataliia Gnyliukh, Walter A. Kaufmann, Vanessa Zheden, Tommaso Costanzo, Pierre Mahou, Mónika Hrtyan, Jie Wang (UGent) , Juan Aguilera-Servin, et al.
(2021) PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 118(51).
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Abstract
Clathrin-mediated endocytosis is the major route of entry of cargos into cells and thus underpins many physiological processes. During endocytosis, an area of flat membrane is remodeled by proteins to create a spherical vesicle against intracellular forces. The protein machinery which mediates this membrane bending in plants is unknown. However, it is known that plant endocytosis is actin independent, thus indicating that plants utilize a unique mechanism to mediate membrane bending against high-turgor pressure compared to other model systems. Here, we investigate the TPLATE complex, a plant-specific endocytosis protein complex. It has been thought to function as a classical adaptor functioning underneath the clathrin coat. However, by using biochemical and advanced live microscopy approaches, we found that TPLATE is peripherally associated with clathrin-coated vesicles and localizes at the rim of endocytosis events. As this localization is more fitting to the protein machinery involved in membrane bending during endocytosis, we examined cells in which the TPLATE complex was disrupted and found that the clathrin structures present as flat patches. This suggests a requirement of the TPLATE complex for membrane bending during plant clathrin–mediated endocytosis. Next, we used in vitro biophysical assays to confirm that the TPLATE complex possesses protein domains with intrinsic membrane remodeling activity. These results redefine the role of the TPLATE complex and implicate it as a key component of the evolutionarily distinct plant endocytosis mechanism, which mediates endocytic membrane bending against the high-turgor pressure in plant cells.
Keywords
Multidisciplinary, clathrin-mediated endocytosis, TPLATE, Arabidopsis, membrane remodeling, TRAFFICKING, ADAPTER, RECRUITMENT, PROTEINS, ACTIN, CHAIN

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MLA
Johnson, Alexander, et al. “The TPLATE Complex Mediates Membrane Bending during Plant Clathrin–Mediated Endocytosis.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 118, no. 51, 2021, doi:10.1073/pnas.2113046118.
APA
Johnson, A., Dahhan, D. A., Gnyliukh, N., Kaufmann, W. A., Zheden, V., Costanzo, T., … Friml, J. (2021). The TPLATE complex mediates membrane bending during plant clathrin–mediated endocytosis. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 118(51). https://doi.org/10.1073/pnas.2113046118
Chicago author-date
Johnson, Alexander, Dana A. Dahhan, Nataliia Gnyliukh, Walter A. Kaufmann, Vanessa Zheden, Tommaso Costanzo, Pierre Mahou, et al. 2021. “The TPLATE Complex Mediates Membrane Bending during Plant Clathrin–Mediated Endocytosis.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 118 (51). https://doi.org/10.1073/pnas.2113046118.
Chicago author-date (all authors)
Johnson, Alexander, Dana A. Dahhan, Nataliia Gnyliukh, Walter A. Kaufmann, Vanessa Zheden, Tommaso Costanzo, Pierre Mahou, Mónika Hrtyan, Jie Wang, Juan Aguilera-Servin, Daniël Van Damme, Emmanuel Beaurepaire, Martin Loose, Sebastian Y. Bednarek, and Jiří Friml. 2021. “The TPLATE Complex Mediates Membrane Bending during Plant Clathrin–Mediated Endocytosis.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 118 (51). doi:10.1073/pnas.2113046118.
Vancouver
1.
Johnson A, Dahhan DA, Gnyliukh N, Kaufmann WA, Zheden V, Costanzo T, et al. The TPLATE complex mediates membrane bending during plant clathrin–mediated endocytosis. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2021;118(51).
IEEE
[1]
A. Johnson et al., “The TPLATE complex mediates membrane bending during plant clathrin–mediated endocytosis,” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 118, no. 51, 2021.
@article{8731758,
  abstract     = {{Clathrin-mediated endocytosis is the major route of entry of cargos into cells and thus underpins many physiological processes. During endocytosis, an area of flat membrane is remodeled by proteins to create a spherical vesicle against intracellular forces. The protein machinery which mediates this membrane bending in plants is unknown. However, it is known that plant endocytosis is actin independent, thus indicating that plants utilize a unique mechanism to mediate membrane bending against high-turgor pressure compared to other model systems. Here, we investigate the TPLATE complex, a plant-specific endocytosis protein complex. It has been thought to function as a classical adaptor functioning underneath the clathrin coat. However, by using biochemical and advanced live microscopy approaches, we found that TPLATE is peripherally associated with clathrin-coated vesicles and localizes at the rim of endocytosis events. As this localization is more fitting to the protein machinery involved in membrane bending during endocytosis, we examined cells in which the TPLATE complex was disrupted and found that the clathrin structures present as flat patches. This suggests a requirement of the TPLATE complex for membrane bending during plant clathrin–mediated endocytosis. Next, we used in vitro biophysical assays to confirm that the TPLATE complex possesses protein domains with intrinsic membrane remodeling activity. These results redefine the role of the TPLATE complex and implicate it as a key component of the evolutionarily distinct plant endocytosis mechanism, which mediates endocytic membrane bending against the high-turgor pressure in plant cells.}},
  articleno    = {{e2113046118}},
  author       = {{Johnson, Alexander and Dahhan, Dana A. and Gnyliukh, Nataliia and Kaufmann, Walter A. and Zheden, Vanessa and Costanzo, Tommaso and Mahou, Pierre and Hrtyan, Mónika and Wang, Jie and Aguilera-Servin, Juan and Van Damme, Daniël and Beaurepaire, Emmanuel and Loose, Martin and Bednarek, Sebastian Y. and Friml, Jiří}},
  issn         = {{0027-8424}},
  journal      = {{PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}},
  keywords     = {{Multidisciplinary,clathrin-mediated endocytosis,TPLATE,Arabidopsis,membrane remodeling,TRAFFICKING,ADAPTER,RECRUITMENT,PROTEINS,ACTIN,CHAIN}},
  language     = {{eng}},
  number       = {{51}},
  pages        = {{9}},
  title        = {{The TPLATE complex mediates membrane bending during plant clathrin–mediated endocytosis}},
  url          = {{http://doi.org/10.1073/pnas.2113046118}},
  volume       = {{118}},
  year         = {{2021}},
}
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