Endosomal membrane budding patterns in plants.

Autor: Weiner E; Center for Quantitative Cell Imaging and Department of Botany, University of Wisconsin-Madison, Madison, WI 53706., Berryman E; Center for Quantitative Cell Imaging and Department of Botany, University of Wisconsin-Madison, Madison, WI 53706., Frey F; Institute of Science and Technology Austria, Klosterneuburg 3400, Austria., Solís AG; Center for Quantitative Cell Imaging and Department of Botany, University of Wisconsin-Madison, Madison, WI 53706., Leier A; Department of Genetics, School of Medicine, University of Alabama-Birmingham, Birmingham, AL 35294-0024., Lago TM; Department of Genetics, School of Medicine, University of Alabama-Birmingham, Birmingham, AL 35294-0024., Šarić A; Institute of Science and Technology Austria, Klosterneuburg 3400, Austria., Otegui MS; Center for Quantitative Cell Imaging and Department of Botany, University of Wisconsin-Madison, Madison, WI 53706.
Jazyk: angličtina
Zdroj: Proceedings of the National Academy of Sciences of the United States of America [Proc Natl Acad Sci U S A] 2024 Oct 29; Vol. 121 (44), pp. e2409407121. Date of Electronic Publication: 2024 Oct 23.
DOI: 10.1073/pnas.2409407121
Abstrakt: 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.
Competing Interests: Competing interests statement:The authors declare no competing interest.
Databáze: MEDLINE