---
OA_place: publisher
OA_type: hybrid
_id: '18526'
abstract:
- lang: eng
text: Multivesicular endosomes (MVEs) sequester membrane proteins destined for degradation
within intralumenal vesicles (ILVs), a process mediated by the membrane-remodeling
action of Endosomal Sorting Complex Required for Transport (ESCRT) proteins. In
Arabidopsis, endosomal membrane constriction and scission are uncoupled, resulting
in the formation of extensive concatenated ILV networks and enhancing cargo sequestration
efficiency. Here, we used a combination of electron tomography, computer simulations,
and mathematical modeling to address the questions of when concatenated ILV networks
evolved in plants and what drives their formation. Through morphometric analyses
of tomographic reconstructions of endosomes across yeast, algae, and various land
plants, we have found that ILV concatenation is widespread within plant species,
but only prevalent in seed plants, especially in flowering plants. Multiple budding
sites that require the formation of pores in the limiting membrane were only identified
in hornworts and seed plants, suggesting that this mechanism has evolved independently
in both plant lineages. To identify the conditions under which these multiple
budding sites can arise, we used particle-based molecular dynamics simulations
and found that changes in ESCRT filament properties, such as filament curvature
and membrane binding energy, can generate the membrane shapes observed in multiple
budding sites. To understand the relationship between membrane budding activity
and ILV network topology, we performed computational simulations and identified
a set of membrane remodeling parameters that can recapitulate our tomographic
datasets.
acknowledgement: We would like to thank Janice Pennington for her support with electron
tomography data collection, Dr. Ingrid Jordon-Thaden, director of the Botany Garden
and Greenhouse of University of Wisconsin Madison, for her invaluable assistance
collecting plant materials, Dr. Marie Trest for providing Chara specimens, and Dr.
Nicholas Keuler for his advice on statistical analyses. We thank Charlie Hamilton
for exploring the initial computational model. This work was supported by grant
NSF MCB 2114603 and NIH 1S10OD026769-01 to M.S.O. F.F acknowledges support as a
NOMIS Fellow from the NOMIS Foundation. A.Š. acknowledges ERC Starting Grant “NEPA”
802960.
article_number: e2409407121
article_processing_charge: Yes (in subscription journal)
article_type: original
author:
- first_name: Ethan
full_name: Weiner, Ethan
last_name: Weiner
- first_name: Elizabeth
full_name: Berryman, Elizabeth
last_name: Berryman
- first_name: Felix F
full_name: Frey, Felix F
id: a0270b37-8f1a-11ec-95c7-8e710c59a4f3
last_name: Frey
orcid: 0000-0001-8501-6017
- first_name: Ariadna González
full_name: Solís, Ariadna González
last_name: Solís
- first_name: André
full_name: Leier, André
last_name: Leier
- first_name: Tatiana Marquez
full_name: Lago, Tatiana Marquez
last_name: Lago
- first_name: Anđela
full_name: Šarić, Anđela
id: bf63d406-f056-11eb-b41d-f263a6566d8b
last_name: Šarić
orcid: 0000-0002-7854-2139
- first_name: Marisa S.
full_name: Otegui, Marisa S.
last_name: Otegui
citation:
ama: Weiner E, Berryman E, Frey FF, et al. Endosomal membrane budding patterns in
plants. Proceedings of the National Academy of Sciences of the United States
of America. 2024;121(44). doi:10.1073/pnas.2409407121
apa: Weiner, E., Berryman, E., Frey, F. F., Solís, A. G., Leier, A., Lago, T. M.,
… Otegui, M. S. (2024). Endosomal membrane budding patterns in plants. Proceedings
of the National Academy of Sciences of the United States of America. National
Academy of Sciences. https://doi.org/10.1073/pnas.2409407121
chicago: Weiner, Ethan, Elizabeth Berryman, Felix F Frey, Ariadna González Solís,
André Leier, Tatiana Marquez Lago, Anđela Šarić, and Marisa S. Otegui. “Endosomal
Membrane Budding Patterns in Plants.” Proceedings of the National Academy of
Sciences of the United States of America. National Academy of Sciences, 2024.
https://doi.org/10.1073/pnas.2409407121.
ieee: E. Weiner et al., “Endosomal membrane budding patterns in plants,”
Proceedings of the National Academy of Sciences of the United States of America,
vol. 121, no. 44. National Academy of Sciences, 2024.
ista: Weiner E, Berryman E, Frey FF, Solís AG, Leier A, Lago TM, Šarić A, Otegui
MS. 2024. Endosomal membrane budding patterns in plants. Proceedings of the National
Academy of Sciences of the United States of America. 121(44), e2409407121.
mla: Weiner, Ethan, et al. “Endosomal Membrane Budding Patterns in Plants.” Proceedings
of the National Academy of Sciences of the United States of America, vol.
121, no. 44, e2409407121, National Academy of Sciences, 2024, doi:10.1073/pnas.2409407121.
short: E. Weiner, E. Berryman, F.F. Frey, A.G. Solís, A. Leier, T.M. Lago, A. Šarić,
M.S. Otegui, Proceedings of the National Academy of Sciences of the United States
of America 121 (2024).
das_tickbox: '1'
dataavailabilitystatement: Electron tomogram files are deposited in EMPIAR under EMPIAR-12299
(54). All other data are included in the manuscript and/or supporting information
date_created: 2024-11-10T23:01:59Z
date_published: 2024-10-29T00:00:00Z
date_updated: 2026-09-24T10:41:24Z
day: '29'
ddc:
- '570'
department:
- _id: AnSa
doi: 10.1073/pnas.2409407121
ec_funded: 1
external_id:
isi:
- '001349500800007'
pmid:
- '39441629'
file:
- access_level: open_access
checksum: 21c82d2ab58ff99b2bd0489797be42e5
content_type: application/pdf
creator: dernst
date_created: 2024-11-11T09:35:15Z
date_updated: 2024-11-11T09:35:15Z
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file_name: 2024_PNAS_Weiner.pdf
file_size: 5268074
relation: main_file
success: 1
file_date_updated: 2024-11-11T09:35:15Z
fulldoi: https://doi.org/10.1073/pnas.2409407121
has_accepted_license: '1'
intvolume: ' 121'
isi: 1
issue: '44'
language:
- iso: eng
license: https://creativecommons.org/licenses/by-nc-nd/4.0/
month: '10'
oa: 1
oa_version: Published Version
pmid: 1
project:
- _id: eba2549b-77a9-11ec-83b8-a81e493eae4e
call_identifier: H2020
grant_number: '802960'
name: 'Non-Equilibrium Protein Assembly: from Building Blocks to Biological Machines'
publication: Proceedings of the National Academy of Sciences of the United States
of America
publication_identifier:
eissn:
- 1091-6490
issn:
- 0027-8424
publication_status: published
publisher: National Academy of Sciences
quality_controlled: '1'
researchdata_availability: yes
scopus_import: '1'
status: public
supplementarymaterial: yes
title: Endosomal membrane budding patterns in plants
tmp:
image: /images/cc_by_nc_nd.png
legal_code_url: https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode
name: Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International
(CC BY-NC-ND 4.0)
short: CC BY-NC-ND (4.0)
type: journal_article
user_id: 317138e5-6ab7-11ef-aa6d-ffef3953e345
volume: 121
year: '2024'
...