Endosomal membrane budding patterns in plants

• 成果类型: Article
• 署名作者: Weiner, Ethan; Berryman, Elizabeth; Frey, Felix; Solis, Ariadna Gonzalez; Leier, Andre; Lago, Tatiana Marquez; Saric, Andela; Otegui, Marisa S.
• 署名单位: University of Wisconsin System; University of Wisconsin Madison; University of Wisconsin System; University of Wisconsin Madison; Institute of Science & Technology - Austria; University of Alabama System; University of Alabama Birmingham
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-8813
• DOI: 10.1073/pnas.2409407121
• 发表日期: 2024-10-29
• 关键词: escrt-iii; arabidopsis; mechanisms; complex; tomography; machinery; interacts; scission; skd1; ist1

摘要

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. Arabidopsis, endosomal membrane constriction and scission are uncoupled, resulting 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 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.