{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T05:11:36Z","timestamp":1790313096893,"version":"4.1.0"},"reference-count":83,"publisher":"American Association for the Advancement of Science (AAAS)","issue":"7","funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["NSF-MCB 1953570"],"award-info":[{"award-number":["NSF-MCB 1953570"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000015","name":"U.S. Department of Energy","doi-asserted-by":"publisher","award":["DE-SC0017160"],"award-info":[{"award-number":["DE-SC0017160"]}],"id":[{"id":"10.13039\/100000015","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000854","name":"International Human Frontier Science Program Organization","doi-asserted-by":"crossref","award":["RGP0005\/2021"],"award-info":[{"award-number":["RGP0005\/2021"]}],"id":[{"id":"10.13039\/501100000854","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Binational Science Foundation","award":["2019330"],"award-info":[{"award-number":["2019330"]}]}],"content-domain":{"domain":["www.science.org"],"crossmark-restriction":true},"short-container-title":["Sci. Adv."],"published-print":{"date-parts":[[2026,2,13]]},"abstract":"<jats:p>\n                    The supramolecular organization of proteins within photosynthetic membranes is crucial for energy conversion in plants. Here, we introduce an analytical and computational pipeline that integrates high-resolution cryo\u2013scanning electron microscopy, biochemical quantification, advanced Monte Carlo computer simulations, and statistical methods to elucidate the elusive protein landscapes of grana membranes in intact\n                    <jats:italic toggle=\"yes\">Arabidopsis<\/jats:italic>\n                    leaves. Our integrated analysis challenges the prevailing view that particles on the exoplasmic fracture faces in freeze-fracture samples represent photosystem II exclusively. Instead, these particles also include cytochrome\n                    <jats:italic toggle=\"yes\">b<\/jats:italic>\n                    <jats:sub>6<\/jats:sub>\n                    <jats:italic toggle=\"yes\">f<\/jats:italic>\n                    complexes. Furthermore, our steric clash analysis demonstrates that stacked membranes contain a mixture of larger PSII supercomplexes (C\n                    <jats:sub>2<\/jats:sub>\n                    S\n                    <jats:sub>2<\/jats:sub>\n                    M\n                    <jats:sub>2<\/jats:sub>\n                    and C\n                    <jats:sub>2<\/jats:sub>\n                    S\n                    <jats:sub>2<\/jats:sub>\n                    ) in addition to a smaller complex (C\n                    <jats:sub>2<\/jats:sub>\n                    ). This suggests that in vivo PSII supercomplexes exist in an equilibrium distribution of differing sizes. Furthermore, we discovered that, although size exclusion effects govern the global protein arrangement, local packing exhibits orientational order indicative of lateral attractive protein-protein interactions.\n                  <\/jats:p>","DOI":"10.1126\/sciadv.aeb2410","type":"journal-article","created":{"date-parts":[[2026,2,11]],"date-time":"2026-02-11T18:58:47Z","timestamp":1770836327000},"update-policy":"https:\/\/doi.org\/10.34133\/aaas_crossmark","source":"Crossref","is-referenced-by-count":3,"title":["Unraveling design principles of protein landscapes in photosynthetic membranes in plant chloroplasts"],"prefix":"10.1126","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6753-7254","authenticated-orcid":true,"given":"Ashraf","family":"Mohamed","sequence":"first","affiliation":[{"name":"Department of Chemistry, University of Texas at Austin, Austin, TX 78712, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuval","family":"Garty","sequence":"additional","affiliation":[{"name":"Department of Biomolecular Sciences, Weizmann Institute of Science, 76100 Rehovot, Israel."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4554-6210","authenticated-orcid":true,"given":"Hui Min Olivia","family":"Oung","sequence":"additional","affiliation":[{"name":"Institute of Biological Chemistry, Washington State University, Pullman, 99164 WA, USA."},{"name":"Department of Plant Biology, University of California, Davis, CA 95616, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7505-4511","authenticated-orcid":true,"given":"Sujith","family":"Puthiyaveetil","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Center for Plant Biology, Purdue University, West Lafayette, IN 47907, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9193-798X","authenticated-orcid":true,"given":"Kajwal K.","family":"Patra","sequence":"additional","affiliation":[{"name":"Department of Chemistry, University of Texas at Austin, Austin, TX 78712, USA."},{"name":"Department of Chemistry, Southern Methodist University, PO Box 750314, Dallas, 75275 TX, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9520-0627","authenticated-orcid":true,"given":"Andrea","family":"Tagliabue","sequence":"additional","affiliation":[{"name":"Department of Chemistry, Southern Methodist University, PO Box 750314, Dallas, 75275 TX, USA."},{"name":"Department of Physics, University of Genoa, 16146 Genoa, Italy."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2749-4229","authenticated-orcid":true,"given":"Steven","family":"Lenhert","sequence":"additional","affiliation":[{"name":"Department of Biological Science, Florida State University, Tallahassee, FL 32306-4370, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0748-7926","authenticated-orcid":true,"given":"Dana","family":"Charuvi","sequence":"additional","affiliation":[{"name":"Institute of Plant Sciences, Agricultural Research Organization, Volcani Institute, Rishon LeZion 7505101, Israel."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0000-3327-4022","authenticated-orcid":true,"given":"Reinat","family":"Nevo","sequence":"additional","affiliation":[{"name":"Department of Chemical Research Support, Weizmann Institute of Science, Rehovot, Israel."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5874-3681","authenticated-orcid":true,"given":"Helmut","family":"Kirchhoff","sequence":"additional","affiliation":[{"name":"Institute of Biological Chemistry, Washington State University, Pullman, 99164 WA, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8322-7371","authenticated-orcid":true,"given":"Doran I. G. B.","family":"Raccah","sequence":"additional","affiliation":[{"name":"Department of Chemistry, University of Texas at Austin, Austin, TX 78712, USA."},{"name":"Department of Chemistry, Southern Methodist University, PO Box 750314, Dallas, 75275 TX, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"221","reference":[{"key":"e_1_3_2_2_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature06523"},{"key":"e_1_3_2_3_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tcb.2016.08.006"},{"key":"e_1_3_2_4_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.03678"},{"key":"e_1_3_2_5_2","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.109.071431"},{"key":"e_1_3_2_6_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbabio.2010.11.007"},{"key":"e_1_3_2_7_2","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.17.00972"},{"key":"e_1_3_2_8_2","doi-asserted-by":"crossref","first-page":"e04889","DOI":"10.7554\/eLife.04889","article-title":"Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography","volume":"4","author":"Engel B. D.","year":"2015","unstructured":"B. D. Engel, M. Schaffer, L. Kuhn Cuellar, E. Villa, J. M. Plitzko, W. Baumeister, Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography. eLife 4, e04889 (2015).","journal-title":"eLife"},{"key":"e_1_3_2_9_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41477-019-0399-7"},{"key":"e_1_3_2_10_2","doi-asserted-by":"publisher","DOI":"10.1104\/pp.110.170647"},{"key":"e_1_3_2_11_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1905994116"},{"key":"e_1_3_2_12_2","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.108.059147"},{"key":"e_1_3_2_13_2","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.105.035030"},{"key":"e_1_3_2_14_2","doi-asserted-by":"publisher","DOI":"10.1016\/S1360-1385(01)02021-0"},{"key":"e_1_3_2_15_2","doi-asserted-by":"publisher","DOI":"10.1016\/0005-2728(80)90078-X"},{"key":"e_1_3_2_16_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbabio.2004.09.009"},{"key":"e_1_3_2_17_2","doi-asserted-by":"publisher","DOI":"10.1111\/tpj.14127"},{"key":"e_1_3_2_18_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.53740"},{"key":"e_1_3_2_19_2","doi-asserted-by":"publisher","DOI":"10.1038\/emboj.2009.232"},{"key":"e_1_3_2_20_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbabio.2012.12.003"},{"key":"e_1_3_2_21_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M600634200"},{"key":"e_1_3_2_22_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M808625200"},{"key":"e_1_3_2_23_2","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.110.081646"},{"key":"e_1_3_2_24_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0005-2728(00)00143-2"},{"key":"e_1_3_2_25_2","doi-asserted-by":"publisher","DOI":"10.1016\/0167-4838(92)90461-L"},{"key":"e_1_3_2_26_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1524999113"},{"key":"e_1_3_2_27_2","doi-asserted-by":"publisher","DOI":"10.1021\/ja403685a"},{"key":"e_1_3_2_28_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1806597115"},{"key":"e_1_3_2_29_2","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2013.00555"},{"key":"e_1_3_2_30_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2019.10.021"},{"key":"e_1_3_2_31_2","doi-asserted-by":"publisher","DOI":"10.1104\/pp.114.255794"},{"key":"e_1_3_2_32_2","first-page":"54066","article-title":"Studying the supramolecular organization of photosynthetic membranes within freeze-fractured leaf tissues by cryo-scanning electron microscopy","author":"Charuvi D.","year":"2016","unstructured":"D. Charuvi, R. Nevo, I. Kaplan-Ashiri, E. Shimoni, Z. Reich, Studying the supramolecular organization of photosynthetic membranes within freeze-fractured leaf tissues by cryo-scanning electron microscopy. J. Vis. Exp., 54066 (2016).","journal-title":"J. Vis. Exp."},{"key":"e_1_3_2_33_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41477-024-01628-9"},{"key":"e_1_3_2_34_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1166299"},{"key":"e_1_3_2_35_2","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.48.3.594"},{"key":"e_1_3_2_36_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0005-2728(89)80215-4"},{"key":"e_1_3_2_37_2","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.71.1.136"},{"key":"e_1_3_2_38_2","doi-asserted-by":"publisher","DOI":"10.1016\/0005-2728(80)90121-8"},{"key":"e_1_3_2_39_2","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.68.1.30"},{"key":"e_1_3_2_40_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF02906493"},{"key":"e_1_3_2_41_2","first-page":"176","article-title":"Further identification of the exoplasmic face particles on the freeze-fractured thylakoid membranes: A study using double and triple mutants from Chlamydomonas reinhardtii lacking various photosystem II subunits and the cytochrome b6\/f complex","volume":"59","author":"Olive J.","year":"1992","unstructured":"J. Olive, M. Recouvreur, J. Girard-Bascou, F. A. Wollman, Further identification of the exoplasmic face particles on the freeze-fractured thylakoid membranes: A study using double and triple mutants from Chlamydomonas reinhardtii lacking various photosystem II subunits and the cytochrome b6\/f complex. Eur. J. Cell Biol. 59, 176\u2013186 (1992).","journal-title":"Eur. J. Cell Biol."},{"key":"e_1_3_2_42_2","doi-asserted-by":"publisher","DOI":"10.1016\/0005-2728(86)90131-3"},{"key":"e_1_3_2_43_2","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.73.2.400"},{"key":"e_1_3_2_44_2","doi-asserted-by":"crossref","unstructured":"L. A. Staehelin \u201cChloroplast structure: From chlorophyll granules to supra-molecular architecture of thylakoid membranes\u201d in Discoveries in Photosynthesis Govindjee J. T. Beatty H. Gest J. F. Allen Eds. (Springer-Verlag Berlin\/Heidelberg 2005; http:\/\/link.springer.com\/10.1007\/1-4020-3324-9_64) vol. 20 of Advances in Photosynthesis and Respiration pp. 717\u2013728.","DOI":"10.1007\/1-4020-3324-9_64"},{"key":"e_1_3_2_45_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-313X.2011.04876.x"},{"key":"e_1_3_2_46_2","doi-asserted-by":"publisher","DOI":"10.1002\/jcb.240240307"},{"key":"e_1_3_2_47_2","doi-asserted-by":"crossref","unstructured":"L. A. Staehelin G. W. M. van der Staay \u201cStructure Composition Functional Organization and Dynamic Properties of Thylakoid Membranes\u201d in Oxygenic Photosynthesis: The Light Reactions D. R. Ort C. F. Yocum I. F. Heichel Eds. (Springer Netherlands Dordrecht 1996; https:\/\/doi.org\/10.1007\/0-306-48127-8_2) pp. 11\u201330.","DOI":"10.1007\/0-306-48127-8_2"},{"key":"e_1_3_2_48_2","doi-asserted-by":"publisher","DOI":"10.1002\/jemt.1060180405"},{"key":"e_1_3_2_49_2","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.87.3.728"},{"key":"e_1_3_2_50_2","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.114.127233"},{"key":"e_1_3_2_51_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbabio.2021.148380"},{"key":"e_1_3_2_52_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbabio.2018.12.005"},{"key":"e_1_3_2_53_2","doi-asserted-by":"publisher","DOI":"10.1021\/bi0494626"},{"key":"e_1_3_2_54_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2005832117"},{"key":"e_1_3_2_55_2","doi-asserted-by":"publisher","DOI":"10.1104\/pp.15.00706"},{"key":"e_1_3_2_56_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.105496"},{"key":"e_1_3_2_57_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbabio.2022.148945"},{"key":"e_1_3_2_58_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bpj.2020.05.034"},{"key":"e_1_3_2_59_2","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.adj0807"},{"key":"e_1_3_2_60_2","doi-asserted-by":"publisher","DOI":"10.1038\/nplants.2017.20"},{"key":"e_1_3_2_61_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbabio.2003.09.004"},{"key":"e_1_3_2_62_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M109.077750"},{"key":"e_1_3_2_63_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bpj.2013.06.052"},{"key":"e_1_3_2_64_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0169-7439(99)00047-7"},{"key":"e_1_3_2_65_2","doi-asserted-by":"publisher","DOI":"10.1021\/bi7017877"},{"key":"e_1_3_2_66_2","doi-asserted-by":"publisher","DOI":"10.1021\/bi700748y"},{"key":"e_1_3_2_67_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbabio.2019.148141"},{"key":"e_1_3_2_68_2","first-page":"11","article-title":"Thylakoid membrane organisation in sun\/shade acclimation","volume":"15","author":"Anderson J. M.","year":"1988","unstructured":"J. M. Anderson, W. S. Chow, D. J. Goodchild, Thylakoid membrane organisation in sun\/shade acclimation. Funct. Plant Biol. 15, 11\u201326 (1988).","journal-title":"Funct. Plant Biol."},{"key":"e_1_3_2_69_2","doi-asserted-by":"publisher","DOI":"10.1016\/0005-2728(93)90134-2"},{"key":"e_1_3_2_70_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jphotobiol.2024.113004"},{"key":"e_1_3_2_71_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbabio.2006.11.019"},{"key":"e_1_3_2_72_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbabio.2015.01.006"},{"key":"e_1_3_2_73_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00425-023-04295-w"},{"key":"e_1_3_2_74_2","doi-asserted-by":"publisher","DOI":"10.1080\/15592324.2016.1218587"},{"key":"e_1_3_2_75_2","doi-asserted-by":"publisher","DOI":"10.1016\/B978-0-12-405210-9.00007-2"},{"key":"e_1_3_2_76_2","doi-asserted-by":"publisher","DOI":"10.1093\/pcp\/pce022"},{"key":"e_1_3_2_77_2","doi-asserted-by":"publisher","DOI":"10.1529\/biophysj.104.045666"},{"key":"e_1_3_2_78_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1413739111"},{"key":"e_1_3_2_79_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2818.1995.tb03635.x"},{"key":"e_1_3_2_80_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41592-019-0582-9"},{"key":"e_1_3_2_81_2","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.2089"},{"key":"e_1_3_2_82_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkr703"},{"key":"e_1_3_2_83_2","unstructured":"S. Gillies C. van der Wel J. Van den Bossche M. W. Taves J. Arnott B. C. Ward Shapely Zenodo. zenodo.15463269 (2025)."},{"key":"e_1_3_2_84_2","unstructured":"S. Kim J. Chen T. Cheng A. Gindulyte J. He S. He Q. Li B. Shoemaker P. Thiessen B. Yu L. Zaslavsky J. Zhang E. Bolton Atomic Radius in the Periodic Table of Elements National Center for Biotechnology Information (2025). https:\/\/pubchem.ncbi.nlm.nih.gov\/periodic-table\/atomic-radius."}],"container-title":["Science Advances"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.science.org\/doi\/pdf\/10.1126\/sciadv.aeb2410","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,2,11]],"date-time":"2026-02-11T18:59:15Z","timestamp":1770836355000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.science.org\/doi\/10.1126\/sciadv.aeb2410"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,2,13]]},"references-count":83,"journal-issue":{"issue":"7","published-print":{"date-parts":[[2026,2,13]]}},"alternative-id":["10.1126\/sciadv.aeb2410"],"URL":"https:\/\/doi.org\/10.1126\/sciadv.aeb2410","relation":{},"ISSN":["2375-2548"],"issn-type":[{"value":"2375-2548","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,2,13]]},"assertion":[{"value":"2025-08-06","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-01-07","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-02-11","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"eaeb2410"}}