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Wetting of phase-separated droplets on plant vacuole membranes leads to a competition between tonoplast budding and nanotube formation

Kusumaatmaja, Halim; May, Alexander I.; Feeney, Mistianne; McKenna, Joseph F.; Mizushima, Noboru; Frigerio, Lorenzo; Knorr, Roland L.

Wetting of phase-separated droplets on plant vacuole membranes leads to a competition between tonoplast budding and nanotube formation Thumbnail


Authors

Alexander I. May

Mistianne Feeney

Joseph F. McKenna

Noboru Mizushima

Lorenzo Frigerio

Roland L. Knorr



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.

Citation

Kusumaatmaja, H., May, A. I., Feeney, M., McKenna, J. F., Mizushima, N., Frigerio, L., & Knorr, R. 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, 118(36), Article e2024109118. https://doi.org/10.1073/pnas.2024109118

Journal Article Type Article
Acceptance Date Aug 4, 2021
Online Publication Date Sep 2, 2021
Publication Date 2021
Deposit Date Oct 18, 2021
Publicly Available Date Mar 29, 2024
Journal Proceedings of the National Academy of Sciences
Print ISSN 0027-8424
Electronic ISSN 1091-6490
Publisher National Academy of Sciences
Peer Reviewed Peer Reviewed
Volume 118
Issue 36
Article Number e2024109118
DOI https://doi.org/10.1073/pnas.2024109118

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