[{"department":[{"_id":"AnSa"}],"title":"Endosomal membrane budding patterns in plants","_id":"18526","publication_identifier":{"issn":["0027-8424"],"eissn":["1091-6490"]},"date_created":"2024-11-10T23:01:59Z","oa_version":"Published Version","pmid":1,"fulldoi":"https://doi.org/10.1073/pnas.2409407121","publication_status":"published","OA_place":"publisher","article_processing_charge":"Yes (in subscription journal)","oa":1,"supplementarymaterial":"yes","publisher":"National Academy of Sciences","type":"journal_article","project":[{"grant_number":"802960","call_identifier":"H2020","name":"Non-Equilibrium Protein Assembly: from Building Blocks to Biological Machines","_id":"eba2549b-77a9-11ec-83b8-a81e493eae4e"}],"year":"2024","language":[{"iso":"eng"}],"abstract":[{"text":"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.","lang":"eng"}],"volume":121,"article_number":"e2409407121","OA_type":"hybrid","date_updated":"2026-09-24T10:41:24Z","intvolume":"       121","file":[{"date_updated":"2024-11-11T09:35:15Z","relation":"main_file","file_name":"2024_PNAS_Weiner.pdf","access_level":"open_access","creator":"dernst","file_id":"18538","content_type":"application/pdf","checksum":"21c82d2ab58ff99b2bd0489797be42e5","file_size":5268074,"date_created":"2024-11-11T09:35:15Z","success":1}],"publication":"Proceedings of the National Academy of Sciences of the United States of America","quality_controlled":"1","month":"10","ddc":["570"],"status":"public","isi":1,"author":[{"last_name":"Weiner","full_name":"Weiner, Ethan","first_name":"Ethan"},{"last_name":"Berryman","first_name":"Elizabeth","full_name":"Berryman, Elizabeth"},{"first_name":"Felix F","full_name":"Frey, Felix F","orcid":"0000-0001-8501-6017","id":"a0270b37-8f1a-11ec-95c7-8e710c59a4f3","last_name":"Frey"},{"full_name":"Solís, Ariadna González","first_name":"Ariadna González","last_name":"Solís"},{"last_name":"Leier","full_name":"Leier, André","first_name":"André"},{"full_name":"Lago, Tatiana Marquez","first_name":"Tatiana Marquez","last_name":"Lago"},{"last_name":"Šarić","full_name":"Šarić, Anđela","orcid":"0000-0002-7854-2139","id":"bf63d406-f056-11eb-b41d-f263a6566d8b","first_name":"Anđela"},{"first_name":"Marisa S.","full_name":"Otegui, Marisa S.","last_name":"Otegui"}],"issue":"44","day":"29","license":"https://creativecommons.org/licenses/by-nc-nd/4.0/","article_type":"original","doi":"10.1073/pnas.2409407121","user_id":"317138e5-6ab7-11ef-aa6d-ffef3953e345","external_id":{"pmid":["39441629"],"isi":["001349500800007"]},"tmp":{"legal_code_url":"https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode","name":"Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0)","image":"/images/cc_by_nc_nd.png","short":"CC BY-NC-ND (4.0)"},"researchdata_availability":"yes","date_published":"2024-10-29T00:00:00Z","acknowledgement":"We would like to thank Janice Pennington for her support with electron tomography data collection, Dr. Ingrid Jordon-Thaden, director of the Botany Garden and Greenhouse of University of Wisconsin Madison, for her invaluable assistance collecting plant materials, Dr. Marie Trest for providing Chara specimens, and Dr. Nicholas Keuler for his advice on statistical analyses. We thank Charlie Hamilton for exploring the initial computational model. This work was supported by grant NSF MCB 2114603 and NIH 1S10OD026769-01 to M.S.O. F.F acknowledges support as a NOMIS Fellow from the NOMIS Foundation. A.Š. acknowledges ERC Starting Grant “NEPA” 802960.","file_date_updated":"2024-11-11T09:35:15Z","has_accepted_license":"1","citation":{"ieee":"E. Weiner <i>et al.</i>, “Endosomal membrane budding patterns in plants,” <i>Proceedings of the National Academy of Sciences of the United States of America</i>, vol. 121, no. 44. National Academy of Sciences, 2024.","ama":"Weiner E, Berryman E, Frey FF, et al. Endosomal membrane budding patterns in plants. <i>Proceedings of the National Academy of Sciences of the United States of America</i>. 2024;121(44). doi:<a href=\"https://doi.org/10.1073/pnas.2409407121\">10.1073/pnas.2409407121</a>","chicago":"Weiner, Ethan, Elizabeth Berryman, Felix F Frey, Ariadna González Solís, André Leier, Tatiana Marquez Lago, Anđela Šarić, and Marisa S. Otegui. “Endosomal Membrane Budding Patterns in Plants.” <i>Proceedings of the National Academy of Sciences of the United States of America</i>. National Academy of Sciences, 2024. <a href=\"https://doi.org/10.1073/pnas.2409407121\">https://doi.org/10.1073/pnas.2409407121</a>.","apa":"Weiner, E., Berryman, E., Frey, F. F., Solís, A. G., Leier, A., Lago, T. M., … Otegui, M. S. (2024). Endosomal membrane budding patterns in plants. <i>Proceedings of the National Academy of Sciences of the United States of America</i>. National Academy of Sciences. <a href=\"https://doi.org/10.1073/pnas.2409407121\">https://doi.org/10.1073/pnas.2409407121</a>","short":"E. Weiner, E. Berryman, F.F. Frey, A.G. Solís, A. Leier, T.M. Lago, A. Šarić, M.S. Otegui, Proceedings of the National Academy of Sciences of the United States of America 121 (2024).","ista":"Weiner E, Berryman E, Frey FF, Solís AG, Leier A, Lago TM, Šarić A, Otegui MS. 2024. Endosomal membrane budding patterns in plants. Proceedings of the National Academy of Sciences of the United States of America. 121(44), e2409407121.","mla":"Weiner, Ethan, et al. “Endosomal Membrane Budding Patterns in Plants.” <i>Proceedings of the National Academy of Sciences of the United States of America</i>, vol. 121, no. 44, e2409407121, National Academy of Sciences, 2024, doi:<a href=\"https://doi.org/10.1073/pnas.2409407121\">10.1073/pnas.2409407121</a>."},"das_tickbox":"1","ec_funded":1,"dataavailabilitystatement":"Electron tomogram files are deposited in EMPIAR under EMPIAR-12299 (54). All other data are included in the manuscript and/or supporting information","scopus_import":"1"}]