{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,19]],"date-time":"2026-05-19T15:43:11Z","timestamp":1779205391645,"version":"3.51.4"},"reference-count":74,"publisher":"Wiley","issue":"12","license":[{"start":{"date-parts":[[2025,12,9]],"date-time":"2025-12-09T00:00:00Z","timestamp":1765238400000},"content-version":"vor","delay-in-days":8,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"},{"start":{"date-parts":[[2025,12,1]],"date-time":"2025-12-01T00:00:00Z","timestamp":1764547200000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["23K19344"],"award-info":[{"award-number":["23K19344"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["23KJ0759"],"award-info":[{"award-number":["23KJ0759"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["23KK0111"],"award-info":[{"award-number":["23KK0111"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["bsppjournals.onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Molecular Plant Pathology"],"published-print":{"date-parts":[[2025,12]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    Recessive resistance, achieved through mutations in host susceptibility genes, offers an effective way for controlling plant viruses. One well\u2010studied gene family involved in such resistance is the\n                    <jats:italic>eukaryotic translation initiation factor 4E<\/jats:italic>\n                    (\n                    <jats:italic>eIF4E<\/jats:italic>\n                    ) gene family, which includes\n                    <jats:italic>eIF4E<\/jats:italic>\n                    ,\n                    <jats:italic>eIFiso4E<\/jats:italic>\n                    and the atypical\n                    <jats:italic>novel cap\u2010binding protein<\/jats:italic>\n                    (\n                    <jats:italic>nCBP<\/jats:italic>\n                    ). Although gene pyramiding of the\n                    <jats:italic>eIF4E<\/jats:italic>\n                    family may provide a promising strategy for broadening virus resistance, it has so far been applied only to a limited set of gene combinations and target viruses. To deepen our understanding of the practicality of\n                    <jats:italic>eIF4E<\/jats:italic>\n                    family gene pyramiding, we analysed a comprehensive set of\n                    <jats:italic>eIF4E<\/jats:italic>\n                    family knockout mutants and six phylogenetically diverse viruses. Double\u2010gene mutant lines\n                    <jats:italic>ncbp eif4e1<\/jats:italic>\n                    and\n                    <jats:italic>ncbp eifiso4e<\/jats:italic>\n                    exhibited resistance to five and three viruses, respectively, due to both additive resistance pyramiding and the emergence of novel resistance resulting from combined mutations. Notably, the observed resistance spectrum included the\n                    <jats:italic>Comovirus<\/jats:italic>\n                    ,\n                    <jats:italic>Tymovirus<\/jats:italic>\n                    ,\n                    <jats:italic>Betacarmovirus<\/jats:italic>\n                    and\n                    <jats:italic>Tobamovirus<\/jats:italic>\n                    genera, which were not previously linked to the\n                    <jats:italic>eIF4E<\/jats:italic>\n                    family. These results reveal a broader involvement of the\n                    <jats:italic>eIF4E<\/jats:italic>\n                    family in viral susceptibility, which may have previously been overlooked due to functional redundancy among the family members. On the other hand, plant growth assessment revealed a more severe penalty in the\n                    <jats:italic>ncbp eif4e1<\/jats:italic>\n                    mutant than in the\n                    <jats:italic>ncbp eifiso4e<\/jats:italic>\n                    mutant, underscoring the need to select compatible gene combinations for resistance pyramiding. Collectively, this study highlights both the advantages and potential drawbacks of\n                    <jats:italic>eIF4E<\/jats:italic>\n                    family gene pyramiding and provides insights for the future development of crop varieties with broad\u2010spectrum virus resistance.\n                  <\/jats:p>","DOI":"10.1111\/mpp.70187","type":"journal-article","created":{"date-parts":[[2025,12,10]],"date-time":"2025-12-10T05:00:20Z","timestamp":1765342820000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Broadening Virus Resistance Through Gene Pyramiding of\n                    <i>eIF4E<\/i>\n                    Family Members"],"prefix":"10.1111","volume":"26","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8393-9587","authenticated-orcid":false,"given":"Masato","family":"Suzuki","sequence":"first","affiliation":[{"name":"Department of Agricultural and Environmental Biology Graduate School of Agricultural and Life Sciences, The University of Tokyo  Tokyo Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Masanobu","family":"Nishikawa","sequence":"additional","affiliation":[{"name":"Department of Agricultural and Environmental Biology Graduate School of Agricultural and Life Sciences, The University of Tokyo  Tokyo Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Toya","family":"Yamamoto","sequence":"additional","affiliation":[{"name":"Department of Agricultural and Environmental Biology Graduate School of Agricultural and Life Sciences, The University of Tokyo  Tokyo Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hiroaki","family":"Koinuma","sequence":"additional","affiliation":[{"name":"Department of Agriculture, School of Agriculture Tokai University  Kumamoto Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Takuya","family":"Keima","sequence":"additional","affiliation":[{"name":"Department of Agricultural and Environmental Biology Graduate School of Agricultural and Life Sciences, The University of Tokyo  Tokyo Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuji","family":"Fujimoto","sequence":"additional","affiliation":[{"name":"College of Science Rikkyo University  Tokyo Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ken","family":"Komatsu","sequence":"additional","affiliation":[{"name":"Graduate School of Agriculture Tokyo University of Agriculture and Technology  Tokyo Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Masayoshi","family":"Hashimoto","sequence":"additional","affiliation":[{"name":"Faculty of Agriculture Shizuoka University  Shizuoka Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yutaro","family":"Neriya","sequence":"additional","affiliation":[{"name":"School of Agriculture Utsunomiya University  Tochigi Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kensaku","family":"Maejima","sequence":"additional","affiliation":[{"name":"Department of Agricultural and Environmental Biology Graduate School of Agricultural and Life Sciences, The University of Tokyo  Tokyo Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1473-4633","authenticated-orcid":false,"given":"Shigetou","family":"Namba","sequence":"additional","affiliation":[{"name":"Department of Agricultural and Environmental Biology Graduate School of Agricultural and Life Sciences, The University of Tokyo  Tokyo Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yasuyuki","family":"Yamaji","sequence":"additional","affiliation":[{"name":"Department of Agricultural and Environmental Biology Graduate School of Agricultural and Life Sciences, The University of Tokyo  Tokyo Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"311","published-online":{"date-parts":[[2025,12,9]]},"reference":[{"key":"e_1_2_10_2_1","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2020.564310"},{"key":"e_1_2_10_3_1","doi-asserted-by":"publisher","DOI":"10.1111\/pbi.12896"},{"key":"e_1_2_10_4_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tplants.2017.01.008"},{"key":"e_1_2_10_5_1","doi-asserted-by":"publisher","DOI":"10.1111\/pbi.13096"},{"key":"e_1_2_10_6_1","doi-asserted-by":"publisher","DOI":"10.1199\/tab.0176"},{"key":"e_1_2_10_7_1","doi-asserted-by":"publisher","DOI":"10.4161\/psb.27940"},{"key":"e_1_2_10_8_1","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.12375"},{"key":"e_1_2_10_9_1","doi-asserted-by":"publisher","DOI":"10.1093\/hr\/uhac159"},{"key":"e_1_2_10_10_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2022.946873"},{"key":"e_1_2_10_11_1","doi-asserted-by":"publisher","DOI":"10.1111\/febs.16275"},{"key":"e_1_2_10_12_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-313X.2002.01481.x"},{"key":"e_1_2_10_13_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-313X.2005.02617.x"},{"key":"e_1_2_10_14_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2023.1143813"},{"key":"e_1_2_10_15_1","doi-asserted-by":"publisher","DOI":"10.1099\/jgv.0.001807"},{"key":"e_1_2_10_16_1","doi-asserted-by":"publisher","DOI":"10.1099\/vir.0.015321-0"},{"key":"e_1_2_10_17_1","doi-asserted-by":"publisher","DOI":"10.1111\/tpj.13136"},{"key":"e_1_2_10_18_1","doi-asserted-by":"publisher","DOI":"10.1111\/pbi.12987"},{"key":"e_1_2_10_19_1","doi-asserted-by":"publisher","DOI":"10.1016\/B978-0-12-809633-8.21339-3"},{"key":"e_1_2_10_20_1","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2016.01695"},{"key":"e_1_2_10_21_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.virol.2009.10.008"},{"key":"e_1_2_10_22_1","doi-asserted-by":"publisher","DOI":"10.1002\/bimj.200810425"},{"key":"e_1_2_10_23_1","doi-asserted-by":"publisher","DOI":"10.1099\/jgv.0.001738"},{"key":"e_1_2_10_24_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1364-3703.2005.00294.x"},{"key":"e_1_2_10_25_1","doi-asserted-by":"publisher","DOI":"10.1038\/srep39678"},{"key":"e_1_2_10_26_1","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.12120"},{"key":"e_1_2_10_27_1","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/erx158"},{"key":"e_1_2_10_28_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00705-013-1635-5"},{"key":"e_1_2_10_29_1","doi-asserted-by":"publisher","DOI":"10.1007\/s12600-022-00991-7"},{"key":"e_1_2_10_30_1","doi-asserted-by":"publisher","DOI":"10.1111\/pbi.14003"},{"key":"e_1_2_10_31_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0960-9822(02)00898-9"},{"key":"e_1_2_10_32_1","doi-asserted-by":"publisher","DOI":"10.1099\/0022-1317-83-8-2085"},{"key":"e_1_2_10_33_1","doi-asserted-by":"publisher","DOI":"10.3390\/ijms252111468"},{"key":"e_1_2_10_34_1","article-title":"Targeted and Random Mutagenesis of Cassava Brown Streak Disease Susceptibility Factors Reveal Molecular Determinants of Disease Severity","volume":"14","author":"Lin Z. J. D.","year":"2025","journal-title":"eLife"},{"key":"e_1_2_10_35_1","doi-asserted-by":"publisher","DOI":"10.1007\/s42994-025-00216-5"},{"key":"e_1_2_10_36_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.hpj.2024.05.001"},{"key":"e_1_2_10_37_1","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2022.873930"},{"key":"e_1_2_10_38_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0029595"},{"key":"e_1_2_10_39_1","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.12422"},{"key":"e_1_2_10_40_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.biochi.2008.03.013"},{"key":"e_1_2_10_41_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1364-3703.2011.00749.x"},{"key":"e_1_2_10_42_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.virol.2019.09.015"},{"key":"e_1_2_10_43_1","doi-asserted-by":"publisher","DOI":"10.1094\/MPMI-11-09-0277"},{"key":"e_1_2_10_44_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.102.017855"},{"key":"e_1_2_10_45_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-313X.2006.02885.x"},{"key":"e_1_2_10_46_1","doi-asserted-by":"publisher","DOI":"10.1128\/jvi.00221-23"},{"key":"e_1_2_10_47_1","doi-asserted-by":"publisher","DOI":"10.1094\/PHYTO.2004.94.7.730"},{"key":"e_1_2_10_48_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.113.227785"},{"key":"e_1_2_10_49_1","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.12417"},{"key":"e_1_2_10_50_1","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.12277"},{"key":"e_1_2_10_51_1","unstructured":"R Core Team.2020.\u201cR: A Language and Environment for Statistical Computing.\u201d"},{"key":"e_1_2_10_52_1","doi-asserted-by":"publisher","DOI":"10.1094\/MPMI-07-12-0174-R"},{"key":"e_1_2_10_53_1","doi-asserted-by":"publisher","DOI":"10.1111\/pbi.14333"},{"key":"e_1_2_10_54_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-313X.2002.01499.x"},{"key":"e_1_2_10_55_1","doi-asserted-by":"publisher","DOI":"10.1099\/vir.0.81817-0"},{"key":"e_1_2_10_56_1","doi-asserted-by":"publisher","DOI":"10.2135\/cropsci2018.08.0518"},{"key":"e_1_2_10_57_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.273.17.10325"},{"key":"e_1_2_10_58_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-94-007-7820-7_2"},{"key":"e_1_2_10_59_1","unstructured":"Schneider G. E.Chicken andR.Becvarik.2024.\u201cNSM3: Functions and Datasets to Accompany Hollander Wolfe and Chicken\u2010Nonparametric Statistical Methods Third Edition.\u201d R Package Version 1.19."},{"key":"e_1_2_10_60_1","doi-asserted-by":"publisher","DOI":"10.1094\/MPMI-04-14-0111-R"},{"key":"e_1_2_10_61_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-313X.2005.02424.x"},{"key":"e_1_2_10_62_1","doi-asserted-by":"publisher","DOI":"10.1016\/0042-6822(91)90123-S"},{"key":"e_1_2_10_63_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.virusres.2005.11.002"},{"key":"e_1_2_10_64_1","doi-asserted-by":"publisher","DOI":"10.1128\/jvi.65.6.2953-2959.1991"},{"key":"e_1_2_10_65_1","doi-asserted-by":"publisher","DOI":"10.1270\/jsbbs.19135"},{"key":"e_1_2_10_66_1","doi-asserted-by":"publisher","DOI":"10.1111\/pbi.14472"},{"key":"e_1_2_10_67_1","doi-asserted-by":"publisher","DOI":"10.21105\/joss.01686"},{"key":"e_1_2_10_68_1","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.78.12.6102-6111.2004"},{"key":"e_1_2_10_69_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-313X.1998.00024.x"},{"key":"e_1_2_10_70_1","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.13031"},{"key":"e_1_2_10_71_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1011417"},{"key":"e_1_2_10_72_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tibtech.2018.04.005"},{"key":"e_1_2_10_73_1","doi-asserted-by":"publisher","DOI":"10.18637\/jss.v096.i01"},{"key":"e_1_2_10_74_1","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.13418"},{"key":"e_1_2_10_75_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2023.1041868"}],"container-title":["Molecular Plant Pathology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/bsppjournals.onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/mpp.70187","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/bsppjournals.onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/mpp.70187","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/bsppjournals.onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/mpp.70187","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,3,8]],"date-time":"2026-03-08T21:24:22Z","timestamp":1773005062000},"score":1,"resource":{"primary":{"URL":"https:\/\/bsppjournals.onlinelibrary.wiley.com\/doi\/10.1111\/mpp.70187"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,12]]},"references-count":74,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2025,12]]}},"alternative-id":["10.1111\/mpp.70187"],"URL":"https:\/\/doi.org\/10.1111\/mpp.70187","archive":["Portico"],"relation":{},"ISSN":["1464-6722","1364-3703"],"issn-type":[{"value":"1464-6722","type":"print"},{"value":"1364-3703","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,12]]},"assertion":[{"value":"2025-08-24","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-11-25","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-12-09","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e70187"}}