{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T12:02:24Z","timestamp":1790164944590,"version":"4.1.0"},"reference-count":100,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T00:00:00Z","timestamp":1790121600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"},{"start":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T00:00:00Z","timestamp":1790121600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32270291"],"award-info":[{"award-number":["32270291"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32470797"],"award-info":[{"award-number":["32470797"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Plant Cell &amp; Environment"],"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    The establishment and maintenance of root nodule symbiosis (RNS) are orchestrated by sophisticated vesicle trafficking networks that coordinate rhizobia infection, nodule organogenesis, and symbiosome development. Central players include Rab and ROP GTPases, soluble\n                    <jats:italic>N<\/jats:italic>\n                    \u2010ethylmaleimide\u2010sensitive factor attachment protein receptors, synaptotagmins, and exocyst complexes, which mediate spatiotemporal membrane identity transitions and enable the formation of a unique nitrogen\u2010fixing organelle termed symbiosome. Additionally, lineage\u2010specific secreted cargoes, such as nodule\u2010specific cysteine\u2010rich peptides in inverted\u2010repeat\u2010lacking clade legumes, drive irreversible bacteroid differentiation and maintain bacteroid viability. Despite developmental architectures diverge across species, a core set of trafficking components is evolutionarily conserved. This review catalogues and contextualises all of endosomal regulators currently known to be required for RNS. We also discuss potential agricultural applications of vesicle trafficking\u2010based strategies in the RNS.\n                  <\/jats:p>","DOI":"10.1111\/pce.70912","type":"journal-article","created":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T11:21:06Z","timestamp":1790162466000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Vesicle Trafficking Orchestrates Root Nodule Symbiosis"],"prefix":"10.1111","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2244-2243","authenticated-orcid":false,"given":"Zhao","family":"Zheng","sequence":"first","affiliation":[{"name":"Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences South China Normal University Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qingren","family":"Liu","sequence":"additional","affiliation":[{"name":"Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences South China Normal University Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0006-4537-5166","authenticated-orcid":false,"given":"Jing","family":"Ren","sequence":"additional","affiliation":[{"name":"HouJi Laboratory in Shanxi Province, College of Agricultural Shanxi Agricultural University Taiyuan China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4084-0808","authenticated-orcid":false,"given":"Chao","family":"Su","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology Huazhong Agricultural University Wuhan China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-7089-259X","authenticated-orcid":false,"given":"Huairong","family":"Pan","sequence":"additional","affiliation":[{"name":"College of Biology Hunan University Changsha China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yixiong","family":"Zheng","sequence":"additional","affiliation":[{"name":"Key Laboratory of Green Prevention and Control on Fruits and Vegetables in South China, Ministry of Agriculture and Rural Affairs, College of Agriculture and Biology Zhongkai University of Agriculture and Engineering Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3788-7883","authenticated-orcid":false,"given":"Zhaosheng","family":"Kong","sequence":"additional","affiliation":[{"name":"HouJi Laboratory in Shanxi Province, College of Agricultural Shanxi Agricultural University Taiyuan China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3958-4499","authenticated-orcid":false,"given":"Caiji","family":"Gao","sequence":"additional","affiliation":[{"name":"Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences South China Normal University Guangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,9,23]]},"reference":[{"issue":"8","key":"e_1_2_5_2_1","doi-asserted-by":"crossref","first-page":"1030","DOI":"10.1016\/j.tplants.2026.03.003","article-title":"Mapping Plant Cell\u2010Type\u2010Specific Responses to Environmental Stresses","volume":"31","author":"Ali M.","year":"2026","journal-title":"Trends in Plant Science"},{"issue":"9","key":"e_1_2_5_3_1","doi-asserted-by":"crossref","first-page":"1138","DOI":"10.1094\/MPMI-20-9-1138","article-title":"Genomic Organization and Evolutionary Insights on GRP and NCR 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W.","year":"2017","journal-title":"Current Biology"},{"issue":"12","key":"e_1_2_5_69_1","doi-asserted-by":"crossref","first-page":"2833","DOI":"10.1105\/tpc.19.00433","article-title":"Remove, Recycle, Degrade: Regulating Plasma Membrane Protein Accumulation","volume":"31","author":"Rodriguez\u2010Furlan C.","year":"2019","journal-title":"Plant Cell"},{"issue":"1","key":"e_1_2_5_70_1","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1105\/tpc.19.00279","article-title":"Celebrating 20 Years of Genetic Discoveries in Legume Nodulation and Symbiotic Nitrogen Fixation","volume":"32","author":"Roy S.","year":"2020","journal-title":"Plant Cell"},{"issue":"3","key":"e_1_2_5_71_1","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1002\/1615-9861(200203)2:3<325::AID-PROT325>3.0.CO;2-W","article-title":"Characterisation by Proteomics of Peribacteroid Space and Peribacteroid Membrane Preparations From Pea (Pisum sativum) Symbiosomes","volume":"2","author":"Saalbach G.","year":"2002","journal-title":"Proteomics"},{"issue":"3","key":"e_1_2_5_72_1","doi-asserted-by":"crossref","first-page":"1508","DOI":"10.1111\/tpj.16871","article-title":"Two Members of a Nodule\u2010Specific Cysteine\u2010Rich (NCR) Peptide Gene Cluster are Required for Differentiation of Rhizobia in Medicago Truncatula Nodules","volume":"119","author":"Saifi F.","year":"2024","journal-title":"Plant Journal"},{"key":"e_1_2_5_73_1","first-page":"1","article-title":"Upright Light\u2010Sheet Microscopy With Two\u2010Photon Excitation for Imaging Large Samples","volume":"33","author":"Saitou T.","year":"2024","journal-title":"Bioimages"},{"key":"e_1_2_5_74_1","article-title":"Developmental Fates and N2\u2010fixing Efficiency of Terminally\u2010Differentiated Versus Undifferentiated Bacteroids From Legume Nodules","volume":"9","author":"Sanchez\u2010Canizares C.","year":"2025","journal-title":"Plant Physiology"},{"issue":"6758","key":"e_1_2_5_75_1","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1038\/46058","article-title":"A Plant Regulator Controlling Development of Symbiotic Root Nodules","volume":"402","author":"Schauser L.","year":"1999","journal-title":"Nature"},{"issue":"12","key":"e_1_2_5_76_1","doi-asserted-by":"crossref","first-page":"1356","DOI":"10.1016\/j.tplants.2024.06.008","article-title":"Unraveling Plant\u2010Microbe Symbioses Using Single\u2010Cell and Spatial Transcriptomics","volume":"29","author":"Serrano K.","year":"2024","journal-title":"Trends in Plant Science"},{"issue":"2","key":"e_1_2_5_77_1","doi-asserted-by":"crossref","DOI":"10.3390\/plants9020276","article-title":"Molecular Basis of Root Nodule Symbiosis Between Bradyrhizobium and \u2018Crack\u2010Entry\u2019 Legume Groundnut (Arachis hypogaea L.)","volume":"9","author":"Sharma V.","year":"2020","journal-title":"Plants"},{"key":"e_1_2_5_78_1","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/j.semcdb.2017.10.005","article-title":"Specificity of Plant Membrane Trafficking \u2010 ARFs, Regulators and Coat Proteins","volume":"80","author":"Singh M. 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