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Wetting of phase-separated droplets on plant vacuole membranes leads to a competition between tonoplast budding and nanotube formation
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Kusumaatmaja, Halim, May, Alexander I., Feeney, Mistianne, McKenna, Joseph F., Mizushima, Noboru, Frigerio, Lorenzo and Knorr, Roland L. (2021) Wetting of phase-separated droplets on plant vacuole membranes leads to a competition between tonoplast budding and nanotube formation. Proceedings of the National Academy of Sciences of the United States of America, 118 (36). e2024109118. doi:10.1073/pnas.2024109118 ISSN 0027-8424.
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Official URL: https://doi.org/10.1073/pnas.2024109118
Abstract
Seeds of dicotyledonous plants store proteins in dedicated membrane-bounded organelles called protein storage vacuoles (PSVs). Formed during seed development through morphological and functional reconfiguration of lytic vacuoles in embryos [M. Feeney et al., Plant Physiol. 177, 241–254 (2018)], PSVs undergo division during the later stages of seed maturation. Here, we study the biophysical mechanism of PSV morphogenesis in vivo, discovering that micrometer-sized liquid droplets containing storage proteins form within the vacuolar lumen through phase separation and wet the tonoplast (vacuolar membrane). We identify distinct tonoplast shapes that arise in response to membrane wetting by droplets and derive a simple theoretical model that conceptualizes these geometries. Conditions of low membrane spontaneous curvature and moderate contact angle (i.e., wettability) favor droplet-induced membrane budding, thereby likely serving to generate multiple, physically separated PSVs in seeds. In contrast, high membrane spontaneous curvature and strong wettability promote an intricate and previously unreported membrane nanotube network that forms at the droplet interface, allowing molecule exchange between droplets and the vacuolar interior. Furthermore, our model predicts that with decreasing wettability, this nanotube structure transitions to a regime with bud and nanotube coexistence, which we confirmed in vitro. As such, we identify intracellular wetting [J. Agudo-Canalejo et al., Nature 591, 142–146 (2021)] as the mechanism underlying PSV morphogenesis and provide evidence suggesting that interconvertible membrane wetting morphologies play a role in the organization of liquid phases in cells.
Item Type: | Journal Article | ||||||||||||||||||
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Subjects: | Q Science > QK Botany | ||||||||||||||||||
Divisions: | Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- ) | ||||||||||||||||||
Library of Congress Subject Headings (LCSH): | Plant vacuoles, Plant proteins, Wetting, Tonoplasts, Budding (Plant propagation), Plants -- Development | ||||||||||||||||||
Journal or Publication Title: | Proceedings of the National Academy of Sciences of the United States of America | ||||||||||||||||||
Publisher: | National Academy of Sciences | ||||||||||||||||||
ISSN: | 0027-8424 | ||||||||||||||||||
Official Date: | 7 September 2021 | ||||||||||||||||||
Dates: |
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Volume: | 118 | ||||||||||||||||||
Number: | 36 | ||||||||||||||||||
Article Number: | e2024109118 | ||||||||||||||||||
DOI: | 10.1073/pnas.2024109118 | ||||||||||||||||||
Status: | Peer Reviewed | ||||||||||||||||||
Publication Status: | Published | ||||||||||||||||||
Access rights to Published version: | Open Access (Creative Commons) | ||||||||||||||||||
Date of first compliant deposit: | 5 August 2021 | ||||||||||||||||||
Date of first compliant Open Access: | 13 September 2021 | ||||||||||||||||||
RIOXX Funder/Project Grant: |
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