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

Wetting of phase-separated droplets on plant vacuole membranes leads to a competition between tonoplast budding and nanotube formation.
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DOI:
10.1073/pnas.2024109118
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发表时间:
2021-09-07
影响因子:
11.1
通讯作者:
Knorr RL
Knorr RL
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Kusumaatmaja H;May AI;Feeney M;McKenna JF;Mizushima N;Frigerio L;Knorr RL

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双子叶植物的种子将蛋白质储存在称为蛋白质储存泡(PSV)的专用膜结合细胞器中。在种子发育过程中通过胚内溶胞的形态和功能重构而形成[M. Feeney等人,177,241-254(2018)],PSV在种子成熟的后期阶段经历分裂。在这里,我们研究了体内PSV形态发生的生物物理机制,发现含有储存蛋白的微米大小的液滴通过相分离在液泡腔内形成,并润湿液泡膜。我们确定不同的液泡膜形状,出现在响应膜润湿液滴,并得出一个简单的理论模型,概念化这些几何形状。低膜自发曲率和中等接触角的条件(即,润湿性)有利于液滴诱导的膜出芽,从而可能用于在种子中产生多个物理分离的PSV。相比之下,高膜自发曲率和强润湿性促进了在液滴界面处形成的复杂且先前未报道的膜纳米管网络,允许液滴和空泡内部之间的分子交换。此外,我们的模型预测,随着润湿性降低,这种纳米管结构过渡到一个政权与芽和纳米管共存,我们在体外证实。因此,我们确定了细胞内润湿[J. Agudo-Canalejo et al.,Nature 591,142-146(2021)]作为PSV形态发生的基础机制,并提供证据表明可互变的膜润湿形态在细胞中液相的组织中起作用。
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.
DOI: 10.1073/pnas.1015892108
发表时间: 2011-03-22
影响因子: 11.1
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