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In this study, we quantified seed Spd content in 208 soybean accessions across two years by RP-HPLC and performed GWAS. Spd showed continuous variation and a high broad-sense heritability (H2 = 0.99). GWAS identified a major repeated locus on chromosome 18, and integrated haplotype and functional analyses prioritized GmSHMT, GmMYB91, and GmCAT9. Favorable haplotypes of these genes were associated with higher Spd content. Promoter analysis revealed common stress-responsive cis elements, and Y1H and dual-LUC assays showed that the MYB transcription factor Glyma.20G223300 directly binds and activates the GmSHMT promoter. Coexpression and RT-qPCR analyses indicated coordinated regulation of Spd biosynthetic genes. Y2H assays further revealed that GmSHMT physically interacts with GmMAT3 and GmSPDS1. Under drought and salt stress, candidate gene expression correlated with Spd accumulation, and favorable haplotypes conferred higher survival. Stable transgenic soybean lines overexpressing GmSHMT showed increased Spd content and enhanced drought and salt tolerance. These findings define a multilayer regulatory network controlling Spd homeostasis and provide genetic targets for stress-resilient soybean breeding.<\/jats:p>","DOI":"10.1021\/acs.jafc.6c11124","type":"journal-article","created":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T05:02:24Z","timestamp":1790226144000},"page":"30676-30692","source":"Crossref","is-referenced-by-count":0,"title":["Integrated GWAS\nand Functional Analyses Reveal a Multi-Layer\nRegulatory Network Orchestrating Spermidine Homeostasis and Stress\nTolerance in Soybean (\n                    <i>Glycine max<\/i>\n                    (L.)\nMerr.)"],"prefix":"10.1021","volume":"74","author":[{"given":"Jie","family":"Wang","sequence":"first","affiliation":[{"name":"Northeast Agricultural University , , ,","place":["Harbin, China, 150030"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xunchao","family":"Zhao","sequence":"additional","affiliation":[{"name":"Northeast Agricultural University , , ,","place":["Harbin, China, 150030"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuan","family":"Li","sequence":"additional","affiliation":[{"name":"Northeast Agricultural University , , ,","place":["Harbin, China, 150030"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shibo","family":"Du","sequence":"additional","affiliation":[{"name":"Northeast Agricultural University , , ,","place":["Harbin, China, 150030"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haiyan","family":"Li","sequence":"additional","affiliation":[{"name":"Northeast Agricultural University , , ,","place":["Harbin, China, 150030"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yongguang","family":"Li","sequence":"additional","affiliation":[{"name":"Northeast Agricultural University , , ,","place":["Harbin, China, 150030"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xue","family":"Zhao","sequence":"additional","affiliation":[{"name":"Northeast Agricultural University , , ,","place":["Harbin, China, 150030"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9829-6588","authenticated-orcid":true,"given":"Yingpeng","family":"Han","sequence":"additional","affiliation":[{"name":"Northeast Agricultural University , , ,","place":["Harbin, China, 150030"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,9,24]]},"reference":[{"key":"2026100711080022400_cit1","doi-asserted-by":"publisher","DOI":"10.59327\/ipcc\/ar6-9789291691647","volume-title":"IPCC, 2023: climate\nChange 2023: synthesis Report. 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Plant Biol."},{"issue":"6","key":"2026100711080022400_cit3","doi-asserted-by":"publisher","first-page":"1237","DOI":"10.1007\/s00425-010-1130-0","article-title":"Polyamines: molecules\nwith regulatory functions in plant abiotic stress tolerance","volume":"231","author":"Alcazar","year":"2010","journal-title":"Planta"},{"key":"2026100711080022400_cit4","doi-asserted-by":"publisher","first-page":"65","DOI":"10.13592\/j.cnki.ppj.1985.06.027","article-title":"Polyamine is the regulator of plant growth\nand development","volume":"6","year":"1985","journal-title":"J. Plant Physiol."},{"issue":"9","key":"2026100711080022400_cit5","doi-asserted-by":"publisher","first-page":"1218","DOI":"10.3390\/plants9091218","article-title":"Transcriptome-Wide Analysis\nof Nitrogen-Regulated Genes in Tea Plant (Camellia sinensis L.O. Kuntze)\nand Characterization of Amino Acid Transporter CsCAT9.1","volume":"9","author":"Zhang","year":"2020","journal-title":"Plants"},{"key":"2026100711080022400_cit6","first-page":"14","article-title":"Regulation\nMechanism of Exogenous\nSpermidine on Resistance of Jujube Tree to High Temperature Stress","volume":"4","author":"Liu","year":"2024","journal-title":"North. Hortic."},{"key":"2026100711080022400_cit7","doi-asserted-by":"publisher","first-page":"1003155","DOI":"10.3389\/fpls.2022.1003155","article-title":"Versatile roles of polyamines\nin improving abiotic stress tolerance of plants","volume":"13","author":"Shao","year":"2022","journal-title":"Front. Plant Sci."},{"issue":"8","key":"2026100711080022400_cit8","doi-asserted-by":"publisher","first-page":"716","DOI":"10.18632\/aging.100361","article-title":"Polyamines in aging and disease","volume":"3","author":"Minois","year":"2011","journal-title":"Aging"},{"key":"2026100711080022400_cit9","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1007\/s00425-008-0772-7","article-title":"Polyamines: Essential\nfactors for growth and survival","volume":"228","author":"Kusano","year":"2008","journal-title":"Planta"},{"issue":"6","key":"2026100711080022400_cit10","doi-asserted-by":"crossref","first-page":"1237","DOI":"10.1007\/s00425-010-1130-0","article-title":"Polyamines: molecules\nwith regulatory functions in plant abiotic\nstress tolerance","volume":"231","author":"Alca\u0301zar","year":"2010","journal-title":"Planta"},{"key":"2026100711080022400_cit11","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.plaphy.2022.07.005","article-title":"Exogenous spermidine\nmodulates polyamine metabolism and improves stress responsive mechanisms\nto protect tomato seedlings against salt stress","volume":"187","author":"Raziq","year":"2022","journal-title":"Plant Physiol. 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Food Chem."},{"key":"2026100711080022400_cit24","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/j.jfca.2016.11.008","article-title":"Soybean spermidine\nconcentration: Genetic and environmental variation of a potential\n\u2018anti-aging\u2019 constituent","volume":"56","author":"Sagara","year":"2017","journal-title":"J. Food\nCompos. Anal."},{"key":"2026100711080022400_cit25","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1007\/978-1-4939-7398-9_35","article-title":"Genome-Wide Association\nMapping Analyses Applied to Polyamines","volume-title":"Polyamines. Methods In Molecular Biology","author":"Barboza-Barquero","year":"2017"},{"key":"2026100711080022400_cit26","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1016\/j.plantsci.2016.02.007","article-title":"Functionality of\nsoybean CBF\/DREB1 transcription factors","volume":"246","author":"Yamasaki","year":"2016","journal-title":"Plant\nSci."},{"key":"2026100711080022400_cit27","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1016\/j.mimet.2018.02.011","article-title":"Extraction of high-quality\nRNA from Bacillus subtilis with a lysozyme pre-treatment followed\nby the Trizol method","volume":"147","author":"Villa-Rodri\u0301guez","year":"2018","journal-title":"J. Microbiol. Methods"},{"issue":"1","key":"2026100711080022400_cit28","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1104\/pp.105.063743","article-title":"Genome-Wide\nIdentification and Testing of Superior\nReference Genes for Transcript Normalization in Arabidopsis","volume":"139","author":"Czechowski","year":"2005","journal-title":"Plant Physiol."},{"issue":"6","key":"2026100711080022400_cit29","doi-asserted-by":"publisher","first-page":"1346","DOI":"10.3390\/agronomy12061346","article-title":"Serine Hydroxymethyltransferase (SHMT) Gene\nFamily in Wheat (Triticum aestivum L.): Identification,\nEvolution, and Expression Analysis","volume":"12","author":"Liu","year":"2022","journal-title":"Agronomy-Basel"},{"key":"2026100711080022400_cit30","doi-asserted-by":"publisher","first-page":"226","DOI":"10.3389\/fgene.2015.00226","article-title":"The molecular cloning\nand clarification of a photorespiratory mutant, oscdm1, using enhancer\ntrapping","volume":"6","author":"Wu","year":"2015","journal-title":"Front. 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Rep."},{"issue":"1","key":"2026100711080022400_cit35","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1104\/pp.109.144220","article-title":"The MYB96\ntranscription\nfactor mediates abscisic acid signaling during drought stress response\nin Arabidopsis","volume":"151","author":"Seo","year":"2009","journal-title":"Plant Physiol."},{"key":"2026100711080022400_cit36","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1186\/1471-2229-12-106","article-title":"Genome-wide analysis\nof the MYB transcription factor superfamily in soybean","volume":"12","author":"Du","year":"2012","journal-title":"BMC Plant Biol."},{"key":"2026100711080022400_cit37","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1016\/j.plaphy.2019.02.010","article-title":"Expression of the maize\nMYB transcription factor ZmMYB3R enhances drought and salt stress\ntolerance in transgenic plants","volume":"137","author":"Wu","year":"2019","journal-title":"Plant Physiol.\nBiochem."},{"key":"2026100711080022400_cit38","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1186\/s12870-022-03829-w","article-title":"Comprehensive genomic characterization of cotton\ncationic amino acid transporter genes reveals that GhCAT10D regulates\nsalt tolerance","volume":"22","author":"Chen","year":"2022","journal-title":"BMC Plant Biol."},{"issue":"23","key":"2026100711080022400_cit39","doi-asserted-by":"publisher","first-page":"12658","DOI":"10.3390\/ijms252312658","article-title":"Genome-Wide Identification\nof the CAT Genes and Molecular Characterization of Their Transcriptional\nResponses to Various Nutrient Stresses in Allotetraploid Rapeseed","volume":"25","author":"Du","year":"2024","journal-title":"Int. J. Mol. Sci."},{"issue":"10","key":"2026100711080022400_cit40","doi-asserted-by":"publisher","first-page":"1938","DOI":"10.1111\/pbi.13111","article-title":"Tea Plant Information\nArchive: a comprehensive genomics and bioinformatics platform for\ntea plant","volume":"17","author":"Xia","year":"2019","journal-title":"Plant Biotechnol. J."},{"issue":"6","key":"2026100711080022400_cit41","doi-asserted-by":"publisher","DOI":"10.1111\/ppl.70649","article-title":"Role of Polyamines\nin Mitigating Salinity Stress in Ornamental and Food Crops","volume":"177","author":"Alagoz","year":"2025","journal-title":"Physiol. Plant"},{"key":"2026100711080022400_cit42","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1007\/978-1-4939-7398-9","article-title":"Quantitative Trait Loci for Root\nGrowth Response to Cadaverine in Arabidopsis","author":"Gibbs","year":"2017","journal-title":"Methods Mol. Biol."},{"issue":"4","key":"2026100711080022400_cit43","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0060325","article-title":"Dissecting\nrice polyamine metabolism under controlled long-term drought stress","volume":"8","author":"Do","year":"2013","journal-title":"PLoS One"},{"key":"2026100711080022400_cit44","doi-asserted-by":"publisher","first-page":"116631","DOI":"10.1016\/j.indcrop.2023.116631","article-title":"Identification\nof QTNs, QEIs interactions and\ngenes for isoflavones in soybean seeds","volume":"197","author":"Yang","year":"2023","journal-title":"Ind.\nCrops Prod."},{"key":"2026100711080022400_cit45","doi-asserted-by":"publisher","first-page":"468","DOI":"10.1016\/j.sajb.2025.06.016","article-title":"Alleviation of vanadium\ntoxicity through individual and combined\nsupplementation of spermine and spermidine in soybean: Insights into\noxidative stress management, detoxification mechanisms, and root exudates","volume":"184","author":"Basit","year":"2025","journal-title":"S. Afr. J. Bot."},{"key":"2026100711080022400_cit46","doi-asserted-by":"publisher","first-page":"1626844","DOI":"10.3389\/fpls.2025.1626844","article-title":"Structure,\nevolution, and roles of MYB transcription\nfactors proteins in secondary metabolite biosynthetic pathways and\nabiotic stresses responses in plants: a comprehensive review","volume":"16","author":"Ma","year":"2025","journal-title":"Front. Plant Sci."},{"key":"2026100711080022400_cit47","doi-asserted-by":"publisher","first-page":"113985","DOI":"10.1016\/j.postharvbio.2025.113985","article-title":"DcCAMTA6-DcCML8 promotes\nGABA accumulation in fresh-cut carrots via transcriptional activation\nof polyamine metabolism genes","volume":"232","author":"Zhang","year":"2026","journal-title":"Postharvest Biol.\nTechnol."},{"key":"2026100711080022400_cit48","doi-asserted-by":"publisher","first-page":"105723","DOI":"10.1016\/j.envexpbot.2024.105723","article-title":"ShWRKY55 enhances the\ncold resistance\nof wild tomato LA1777 by regulating the expression of the key gene ShSAMDC2 involved in polyamine synthesis","volume":"221","author":"Zhang","year":"2024","journal-title":"Environ. Exp. Bot."},{"key":"2026100711080022400_cit49","doi-asserted-by":"publisher","first-page":"109537","DOI":"10.1016\/j.plaphy.2025.109537","article-title":"The basic helix-loop-helix\ntranscription factor PpeUNE12\nregulates peach ripening by promoting polyamine catabolism and anthocyanin\nsynthesis","volume":"220","author":"Wang","year":"2025","journal-title":"Plant Physiol. Biochem."},{"issue":"6","key":"2026100711080022400_cit50","doi-asserted-by":"publisher","first-page":"1435","DOI":"10.1111\/pbi.14278","article-title":"Metabolite-based\ngenome-wide\nassociation studies enable the dissection of the genetic bases of\nflavonoids, betaine and spermidine in wolfberry (Lycium)","volume":"22","author":"Zhao","year":"2024","journal-title":"Plant Biotechnol. J."}],"container-title":["Journal of Agricultural\nand Food Chemistry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acs.jafc.6c11124","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/jafcau\/article-pdf\/74\/39\/30676\/68632320\/acs.jafc.6c11124.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/jafcau\/article-pdf\/74\/39\/30676\/68632320\/acs.jafc.6c11124.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T15:37:05Z","timestamp":1791387425000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/jafcau\/article\/74\/39\/30676\/5437292\/Integrated-GWAS-and-Functional-Analyses-Reveal-a"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,24]]},"references-count":50,"journal-issue":{"issue":"39","published-online":{"date-parts":[[2026,9,24]]},"published-print":{"date-parts":[[2026,10,7]]}},"URL":"https:\/\/doi.org\/10.1021\/acs.jafc.6c11124","relation":{},"ISSN":["0021-8561","1520-5118"],"issn-type":[{"value":"0021-8561","type":"print"},{"value":"1520-5118","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,24]]}}}