{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T12:47:58Z","timestamp":1792068478682,"version":"4.4.0"},"reference-count":51,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T00:00:00Z","timestamp":1792022400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"},{"start":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T00:00:00Z","timestamp":1792022400000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["JIPB"],"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    Soybean (\n                    <jats:italic>Glycine max<\/jats:italic>\n                    [L.] Merr.) was domesticated in China over five millennia ago; yet, its global expansion has resulted in two distinct, independently evolved breeding pools in China and the Americas. While regional breeding has optimized specific traits, a comprehensive roadmap for the reciprocal exchange of these \u201cbreeding\u2010specific\u201d beneficial alleles is lacking. Here, we performed a large\u2010scale genomic dissection of 2,377 soybean accessions, integrating 8.4 million high\u2010quality SNPs with multi\u2010environment phenotyping across 11 locations. Through genome\u2010wide association studies (GWAS), we identified 261 significant loci (223 novel) governing six key agronomic traits, revealing that Chinese and American germplasms have accumulated distinct sets of beneficial alleles of seed size\/protein in China and oil\/yield in the Americas. To harness this untapped potential, we developed the Soybean Targeted Improvement Navigation System (STINS), a framework integrating population genomics, GWAS, and genomic selection (GS). We demonstrate the potential of targeted beneficial allele introgression between populations via gene modification for rapid trait improvement. Proof\u2010of\u2010concept functional evaluation through CRISPR\/Cas9\u2010mediated knockout of\n                    <jats:italic>GmST05<\/jats:italic>\n                    in an American cultivar and overexpression of a resistant\n                    <jats:italic>GmSNAP18<\/jats:italic>\n                    haplotype in a Chinese cultivar provided experimental support for STINS\u2010predicted targets for protein content and SCN resistance improvement. Our study provides a navigable genomic resource for \u201cknowledge\u2010driven design breeding\u201d, offering a blueprint for the global exchange of elite alleles to ensure future food security.\n                  <\/jats:p>","DOI":"10.1111\/jipb.70421","type":"journal-article","created":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T11:59:36Z","timestamp":1792065576000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Genomic dissection of divergent selection reveals a roadmap for reciprocal improvement of Chinese and American soybean"],"prefix":"10.1111","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7037-5217","authenticated-orcid":false,"given":"Chengzhi","family":"Jiao","sequence":"first","affiliation":[{"name":"Key Laboratory of Grain Crop Genetic Resources Evaluation and Utilization (MARA), Institute of Crop Sciences Chinese Academy of Agricultural Sciences Beijing 100081 China"},{"name":"State Key Laboratory of Wheat Improvement, Shandong Laboratory of Advanced Agricultural Sciences Peking University Institute of Advanced Agricultural Sciences Weifang 261325 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3689-3790","authenticated-orcid":false,"given":"Delin","family":"Li","sequence":"additional","affiliation":[{"name":"Key Laboratory of Grain Crop Genetic Resources Evaluation and Utilization (MARA), Institute of Crop Sciences Chinese Academy of Agricultural Sciences Beijing 100081 China"},{"name":"Xianghu Laboratory Hangzhou 311231 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0003-0723-6964","authenticated-orcid":false,"given":"Hao","family":"Zhang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Grain Crop Genetic Resources Evaluation and Utilization (MARA), Institute of Crop Sciences Chinese Academy of Agricultural Sciences Beijing 100081 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4996-7912","authenticated-orcid":false,"given":"Zhongren","family":"Zhang","sequence":"additional","affiliation":[{"name":"Smartgenomics Technology Institute Qingdao 266111 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-9388-4656","authenticated-orcid":false,"given":"Xueqing","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Grain Crop Genetic Resources Evaluation and Utilization (MARA), Institute of Crop Sciences Chinese Academy of Agricultural Sciences Beijing 100081 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0001-0655-515X","authenticated-orcid":false,"given":"Long","family":"Yan","sequence":"additional","affiliation":[{"name":"Institute of Cereal and Oil Crops Hebei Academy of Agriculture and Forestry Sciences Shijiazhuang 050031 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-9455-222X","authenticated-orcid":false,"given":"Tianqing","family":"Zheng","sequence":"additional","affiliation":[{"name":"Key Laboratory of Grain Crop Genetic Resources Evaluation and Utilization (MARA), Institute of Crop Sciences Chinese Academy of Agricultural Sciences Beijing 100081 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6298-8796","authenticated-orcid":false,"given":"Chaosen","family":"Zhao","sequence":"additional","affiliation":[{"name":"Crops Research, Institute of Jiangxi Academy of Agricultural Sciences Nanchang 330200 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6951-0218","authenticated-orcid":false,"given":"Hongmei","family":"Qiu","sequence":"additional","affiliation":[{"name":"Soybean Research Institute Jilin Academy of Agricultural Sciences Changchun 130033 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2507-9195","authenticated-orcid":false,"given":"Guangnan","family":"Xing","sequence":"additional","affiliation":[{"name":"Soybean Research Institute Nanjing Agricultural University Nanjing 210095 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-3537-849X","authenticated-orcid":false,"given":"Guoyu","family":"Hu","sequence":"additional","affiliation":[{"name":"Crop Institute of Anhui Academy of Agricultural Sciences Hefei 230031 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-1481-7065","authenticated-orcid":false,"given":"Like","family":"Liu","sequence":"additional","affiliation":[{"name":"School of Life Sciences Liaocheng University Liaocheng 252059 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-0197-4532","authenticated-orcid":false,"given":"Qiang","family":"Wang","sequence":"additional","affiliation":[{"name":"Institute of Crop Resources Heilongjiang Academy of Agricultural Sciences Harbin 150086 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0000-3778-0520","authenticated-orcid":false,"given":"Wen","family":"Huang","sequence":"additional","affiliation":[{"name":"Tong Hua Academy of Agricultural Sciences Meihekou 135007 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9214-2385","authenticated-orcid":false,"given":"Xing","family":"Wang","sequence":"additional","affiliation":[{"name":"Xuzhou Institute of Agricultural Sciences in XuHuai Region of Jiangsu Xuzhou 221131 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-7261-7084","authenticated-orcid":false,"given":"Yumin","family":"Wang","sequence":"additional","affiliation":[{"name":"Soybean Research Institute Jilin Academy of Agricultural Sciences Changchun 130033 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0000-5470-2882","authenticated-orcid":false,"given":"Long","family":"Miao","sequence":"additional","affiliation":[{"name":"School of Agronomy Anhui Agricultural University Hefei 230036 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5566-7222","authenticated-orcid":false,"given":"YanFei","family":"Li","sequence":"additional","affiliation":[{"name":"Key Laboratory of Grain Crop Genetic Resources Evaluation and Utilization (MARA), Institute of Crop Sciences Chinese Academy of Agricultural Sciences Beijing 100081 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Chinese Academy of Agricultural Sciences Beijing 100081 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8940-1924","authenticated-orcid":false,"given":"Ying\u2010Hui","family":"Li","sequence":"additional","affiliation":[{"name":"Key Laboratory of Grain Crop Genetic Resources Evaluation and Utilization (MARA), Institute of Crop Sciences Chinese Academy of Agricultural Sciences Beijing 100081 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2810-9249","authenticated-orcid":false,"given":"Xiaobo","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Grain Crop Genetic Resources Evaluation and Utilization (MARA), Institute of Crop Sciences Chinese Academy of Agricultural Sciences Beijing 100081 China"},{"name":"School of Agronomy Anhui Agricultural University Hefei 230036 China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5777-3344","authenticated-orcid":false,"given":"Li\u2010Juan","family":"Qiu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Grain Crop Genetic Resources Evaluation and Utilization (MARA), Institute of Crop Sciences Chinese Academy of Agricultural Sciences Beijing 100081 China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,10,15]]},"reference":[{"key":"e_1_2_9_2_1","doi-asserted-by":"crossref","first-page":"1655","DOI":"10.1101\/gr.094052.109","article-title":"Fast model\u2010based estimation of ancestry in unrelated individuals","volume":"19","author":"Alexander D.H.","year":"2009","journal-title":"Genome Res."},{"key":"e_1_2_9_3_1","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1094\/PHP-RS-16-0066","article-title":"Soybean yield loss estimates due to diseases in the United States and Ontario, Canada, from 2010 to 2014","volume":"18","author":"Allen T.W.","year":"2017","journal-title":"Plant Health Prog."},{"key":"e_1_2_9_4_1","doi-asserted-by":"crossref","first-page":"E7375","DOI":"10.1073\/pnas.1610150113","article-title":"Disease resistance through impairment of \u03b1\u2010SNAP\u2013NSF interaction and vesicular trafficking by soybean Rhg1","volume":"113","author":"Bayless A.M.","year":"2016","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_2_9_5_1","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.biotechadv.2014.12.006","article-title":"The CRISPR\/Cas9 system for plant genome editing and beyond","volume":"33","author":"Bortesi L.","year":"2015","journal-title":"Biotechnol. Adv."},{"key":"e_1_2_9_6_1","doi-asserted-by":"crossref","first-page":"2368","DOI":"10.1111\/jipb.13561","article-title":"Natural variation of GmFATA1B regulates seed oil content and composition in soybean","volume":"65","author":"Cai Z.","year":"2023","journal-title":"J. Integr. Plant Biol."},{"key":"e_1_2_9_7_1","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1111\/nph.18792","article-title":"MOTHER\u2010OF\u2010FT\u2010AND\u2010TFL1 regulates the seed oil and protein content in soybean","volume":"239","author":"Cai Z.","year":"2023","journal-title":"New Phytol."},{"key":"e_1_2_9_8_1","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1016\/j.molp.2021.10.004","article-title":"Parallel selection of distinct Tof5 alleles drove the adaptation of cultivated and wild soybean to high latitudes","volume":"15","author":"Dong L.","year":"2022","journal-title":"Mol. Plant"},{"key":"e_1_2_9_9_1","doi-asserted-by":"crossref","first-page":"5445","DOI":"10.1038\/s41467-021-25800-3","article-title":"Genetic basis and adaptation trajectory of soybean from its temperate origin to tropics","volume":"12","author":"Dong L.","year":"2021","journal-title":"Nat. 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Genet."},{"key":"e_1_2_9_13_1","doi-asserted-by":"crossref","first-page":"3051","DOI":"10.1038\/s41467-022-30314-7","article-title":"POWR1 is a domestication gene pleiotropically regulating seed quality and yield in soybean","volume":"13","author":"Goettel W.","year":"2022","journal-title":"Nat. Commun."},{"key":"e_1_2_9_14_1","doi-asserted-by":"crossref","first-page":"2669","DOI":"10.1021\/jf0014009","article-title":"Comparison of quality characteristics of soybeans from Brazil, China, and the United States","volume":"49","author":"Grieshop C.","year":"2001","journal-title":"J. Agric. Food Chem."},{"key":"e_1_2_9_15_1","doi-asserted-by":"crossref","first-page":"1745","DOI":"10.1038\/s41588-023-01495-8","article-title":"Structure and function of rice hybrid genomes reveal genetic basis and optimal performance of heterosis","volume":"55","author":"Gu Z.","year":"2023","journal-title":"Nat. Genet."},{"key":"e_1_2_9_16_1","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1002\/csc2.20110","article-title":"Designing crops for adaptation to the drought and high\u2010temperature risks anticipated in future climates","volume":"60","author":"Hammer G.L.","year":"2020","journal-title":"Crop Sci."},{"key":"e_1_2_9_17_1","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1111\/nph.18153","article-title":"Downregulation of a gibberellin 3\u03b2\u2010hydroxylase enhances photosynthesis and increases seed yield in soybean","volume":"235","author":"Hu D.","year":"2022","journal-title":"New Phytol."},{"key":"e_1_2_9_18_1","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2205783119","article-title":"The genomics of linkage drag in inbred lines of sunflower","volume":"120","author":"Huang K.","year":"2023","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_2_9_19_1","doi-asserted-by":"crossref","first-page":"16666","DOI":"10.1073\/pnas.0604379103","article-title":"Impacts of genetic bottlenecks on soybean genome diversity","volume":"103","author":"Hyten D.L.","year":"2006","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_2_9_20_1","doi-asserted-by":"crossref","first-page":"4807","DOI":"10.1105\/tpc.112.104968","article-title":"Ln is a key regulator of leaflet shape and number of seeds per pod in soybean","volume":"24","author":"Jeong N.","year":"2012","journal-title":"Plant Cell"},{"key":"e_1_2_9_21_1","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1007\/s00122-018-3271-7","article-title":"Genetic diversity patterns and domestication origin of soybean","volume":"132","author":"Jeong S.C.","year":"2019","journal-title":"Theor. Appl. 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China Life Sci."},{"key":"e_1_2_9_27_1","first-page":"1","article-title":"Dissecting the genetic basis of resistance to soybean cyst nematode combining linkage and association mapping","volume":"9","author":"Li Y.","year":"2016","journal-title":"Plant Genome"},{"key":"e_1_2_9_28_1","doi-asserted-by":"crossref","first-page":"6429","DOI":"10.1038\/s41467-022-34153-4","article-title":"Natural variation of Dt2 determines branching in soybean","volume":"13","author":"Liang Q.","year":"2022","journal-title":"Nat. Commun."},{"key":"e_1_2_9_29_1","doi-asserted-by":"crossref","first-page":"3773","DOI":"10.1007\/s00122-022-04101-3","article-title":"Breeding for disease resistance in soybean: A global perspective","volume":"135","author":"Lin F.","year":"2022","journal-title":"Theor. Appl. Genet."},{"key":"e_1_2_9_30_1","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1104\/pp.109.150607","article-title":"The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER1","volume":"153","author":"Liu B.","year":"2010","journal-title":"Plant Physiol."},{"key":"e_1_2_9_31_1","doi-asserted-by":"crossref","DOI":"10.1038\/ncomms14822","article-title":"The soybean GmSNAP18 gene underlies two types of resistance to soybean cyst nematode","volume":"8","author":"Liu S.","year":"2017","journal-title":"Nat. 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Genet."},{"key":"e_1_2_9_38_1","doi-asserted-by":"crossref","first-page":"6813","DOI":"10.1038\/s41467-023-42608-5","article-title":"PH13 improves soybean shade traits and enhances yield for high\u2010density planting at high latitudes","volume":"14","author":"Qin C.","year":"2023","journal-title":"Nat. Commun."},{"key":"e_1_2_9_39_1","volume-title":"Descriptors and data standard for soybean","author":"Qiu L.","year":"2006"},{"key":"e_1_2_9_40_1","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1017\/S1479262110000493","article-title":"The worldwide utilization of the Chinese soybean germplasm collection","volume":"9","author":"Qiu L.","year":"2011","journal-title":"Plant Genet. Resour."},{"key":"e_1_2_9_41_1","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1038\/nature08670","article-title":"Genome sequence of the palaeopolyploid soybean","volume":"463","author":"Schmutz J.","year":"2010","journal-title":"Nature"},{"key":"e_1_2_9_42_1","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1093\/aob\/mct269","article-title":"Natural variation in the genes responsible for maturity loci E1, E2, E3 and E4 in soybean","volume":"113","author":"Tsubokura Y.","year":"2014","journal-title":"Ann. Bot."},{"key":"e_1_2_9_43_1","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1101\/gr.073585.107","article-title":"EnsemblCompara GeneTrees: Complete, duplication\u2010aware phylogenetic trees in vertebrates","volume":"19","author":"Vilella A.J.","year":"2009","journal-title":"Genome Res."},{"key":"e_1_2_9_44_1","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1007\/s00122-015-2474-4","article-title":"QTL for seed protein and amino acids in the Benning \u00d7 Danbaekkong soybean population","volume":"128","author":"Warrington C.V.","year":"2015","journal-title":"Theor. Appl. Genet."},{"key":"e_1_2_9_45_1","doi-asserted-by":"crossref","first-page":"1711","DOI":"10.2135\/cropsci2001.1711","article-title":"Sixty years of improvement in publicly developed elite soybean lines","volume":"41","author":"Wilcox J.R.","year":"2001","journal-title":"Crop Sci."},{"key":"e_1_2_9_46_1","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1186\/s12870-014-0327-y","article-title":"A CRISPR\/Cas9 toolkit for multiplex genome editing in plants","volume":"14","author":"Xing H.","year":"2014","journal-title":"BMC Plant Biol."},{"key":"e_1_2_9_47_1","doi-asserted-by":"crossref","first-page":"4059","DOI":"10.3390\/foods11244059","article-title":"Can soybean cultivars with larger seed size produce more protein, lipids, and seed yield? 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