{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T14:15:28Z","timestamp":1789049728377,"version":"build-2803163510"},"reference-count":42,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T00:00:00Z","timestamp":1788998400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"},{"start":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T00:00:00Z","timestamp":1788998400000},"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":["Plant Cell &amp; Environment"],"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    Stem architecture is a major determinant of lodging resistance, biomass accumulation, and harvest efficiency in soybean. However, the molecular features associated with contrasting stem growth habits in wild soybean remain incompletely characterised. Here, we performed an integrated transcriptomic, metabolomic, and epigenomic analysis of stem growth\u2010habit divergence in wild soybean, comparing the wild\u2010type accession ZYD7068 with contrasting vining and erect mutant lines derived from carbon\u2010ion beam mutagenesis. Pairwise transcriptomic comparisons identified between 20\u2009311 and 28\u2009705 differentially expressed genes per contrast, with a core set of 2672 genes consistently altered across the comparisons. Functional enrichment, gene set variation analysis, and gene set enrichment analysis converged on xylem and phloem pattern formation as a prominent molecular pathway associated with growth\u2010habit divergence. Random forest analysis identified BBR\u2010BPC and ARF transcription factor families as major molecular discriminators, while metabolomic profiling revealed distinct metabolic profiles involving amino\u2010acid\u2010derived and lipid\u2010associated metabolites. Whole\u2010genome bisulfite sequencing revealed context\u2010specific DNA methylation differences, including substantial variation in CHG methylation among erect mutant lines. Integrated network and in silico perturbation analyses prioritised four candidate genes associated with vascular development for future functional validation. Together, these results provide a multi\u2010layer molecular resource for investigating stem growth\u2010habit divergence in\n                    <jats:italic>G. soja<\/jats:italic>\n                    and establish testable candidate pathways and genes for subsequent functional studies and soybean improvement.\n                  <\/jats:p>","DOI":"10.1111\/pce.70872","type":"journal-article","created":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T13:50:08Z","timestamp":1789048208000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Integrative Multi\u2010Omics Analysis of Stem Growth Habit Divergence in Wild Soybean (\n                    <i>Glycine soja<\/i>\n                    )"],"prefix":"10.1111","author":[{"given":"Xiulin","family":"Liu","sequence":"first","affiliation":[{"name":"Soybean Research Institute of Heilongjiang Academy of Agriculture Sciences Harbin China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xueyang","family":"Wang","sequence":"additional","affiliation":[{"name":"Soybean Research Institute of Heilongjiang Academy of Agriculture Sciences Harbin China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huilong","family":"Hong","sequence":"additional","affiliation":[{"name":"National Key Facility for Gene Resources and Genetic Improvement\/Key Laboratory of Crop Germplasm Utilization Ministry of Agriculture, Institute of Crop Science, Chinese Academy of Agricultural Sciences Beijing China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kenzhen","family":"Zhao","sequence":"additional","affiliation":[{"name":"Soybean Research Institute of Heilongjiang Academy of Agriculture Sciences Harbin China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunlei","family":"Zhang","sequence":"additional","affiliation":[{"name":"Soybean Research Institute of Heilongjiang Academy of Agriculture Sciences Harbin China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fengyi","family":"Zhang","sequence":"additional","affiliation":[{"name":"Soybean Research Institute of Heilongjiang Academy of Agriculture Sciences Harbin China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5716-8208","authenticated-orcid":false,"given":"Rongqiang","family":"Yuan","sequence":"additional","affiliation":[{"name":"Soybean Research Institute of Heilongjiang Academy of Agriculture Sciences Harbin China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dai","family":"Shi","sequence":"additional","affiliation":[{"name":"Fujing Agricultural Socialized Service Center Jiamushi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5003-9275","authenticated-orcid":false,"given":"Sobhi F.","family":"Lamlom","sequence":"additional","affiliation":[{"name":"Soybean Research Institute of Heilongjiang Academy of Agriculture Sciences Harbin China"},{"name":"Plant Production Department Faculty of Agriculture Saba Basha, Alexandria University Alexandria Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bixian","family":"Zhang","sequence":"additional","affiliation":[{"name":"Soybean Research Institute of Heilongjiang Academy of Agriculture Sciences Harbin China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-6846-3479","authenticated-orcid":false,"given":"Honglei","family":"Ren","sequence":"additional","affiliation":[{"name":"Soybean Research Institute of Heilongjiang Academy of Agriculture Sciences Harbin China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,9,10]]},"reference":[{"issue":"19","key":"e_1_2_11_2_1","doi-asserted-by":"crossref","first-page":"3711","DOI":"10.1007\/s00018-020-03496-w","article-title":"Plant Vascular Development: Mechanisms and Environmental Regulation","volume":"77","author":"Agust\u00ed J.","year":"2020","journal-title":"Cellular and Molecular Life Sciences"},{"issue":"4","key":"e_1_2_11_3_1","first-page":"60","article-title":"Plant Cuticular Waxes: A Review on Functions, Composition, Biosyntheses Mechanism and Transportation","volume":"12","author":"Ahmad H. M.","year":"2015","journal-title":"Life Sci J"},{"key":"e_1_2_11_4_1","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/B978-0-443-33064-3.00008-6","volume-title":"Transcriptomics in Atherosclerosis","author":"Alexiou P.","year":"2026"},{"key":"e_1_2_11_5_1","doi-asserted-by":"crossref","first-page":"189","DOI":"10.3389\/fpls.2013.00189","article-title":"Identification of Novel Transcription Factors Regulating Secondary Cell Wall Formation in Arabidopsis","volume":"4","author":"Cassan\u2010Wang H.","year":"2013","journal-title":"Frontiers in Plant Science"},{"issue":"12","key":"e_1_2_11_6_1","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1007\/s00122-023-04493-w","article-title":"Identification and Mapping of a Recessive Allele, dt3, Specifying Semideterminate Stem Growth Habit in Soybean","volume":"136","author":"Clark C. B.","year":"2023","journal-title":"Theoretical and Applied Genetics"},{"issue":"4","key":"e_1_2_11_7_1","doi-asserted-by":"crossref","first-page":"1466","DOI":"10.3390\/ijms26041466","article-title":"Integrative Multi\u2010Omics Approaches for Identifying and Characterizing Biological Elements in Crop Traits: Current Progress and Future Prospects","volume":"26","author":"Fan B.\u2010L.","year":"2025","journal-title":"International Journal of Molecular Sciences"},{"issue":"4","key":"e_1_2_11_8_1","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1016\/j.molp.2025.02.003","article-title":"A Large\u2010Scale Integrated Transcriptomic Atlas for Soybean Organ Development","volume":"18","author":"Fan J.","year":"2025","journal-title":"Molecular Plant"},{"issue":"5","key":"e_1_2_11_9_1","doi-asserted-by":"crossref","first-page":"671","DOI":"10.3390\/plants14050671","article-title":"Integrative Approaches to Soybean Resilience, Productivity, and Utility: A Review of Genomics, Computational Modeling, and Economic Viability","volume":"14","author":"Gai Y.","year":"2025","journal-title":"Plants"},{"issue":"11","key":"e_1_2_11_10_1","doi-asserted-by":"crossref","first-page":"4095","DOI":"10.1007\/s00122-022-04222-9","article-title":"Soybean Genetic Resources Contributing to Sustainable Protein Production","volume":"135","author":"Guo B.","year":"2022","journal-title":"Theoretical and Applied Genetics"},{"issue":"19","key":"e_1_2_11_11_1","doi-asserted-by":"crossref","first-page":"2714","DOI":"10.3390\/plants13192714","article-title":"Harnessing Multi\u2010Omics Strategies and Bioinformatics Innovations for Advancing Soybean Improvement: A Comprehensive Review","volume":"13","author":"Haidar S.","year":"2024","journal-title":"Plants"},{"issue":"3","key":"e_1_2_11_12_1","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1104\/pp.15.00409","article-title":"The Arabidopsis Gaga\u2010Binding Factor Basic pentacysteine6 Recruits the Polycomb\u2010Repressive complex1 Component Like Heterochromatin protein1 to Gaga DNA Motifs","volume":"168","author":"Hecker A.","year":"2015","journal-title":"Plant Physiology"},{"issue":"05","key":"e_1_2_11_13_1","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1055\/s-2003-44780","article-title":"Between Xylem and Phloem: The Genetic Control of Cambial Activity in Plants","volume":"5","author":"Helariutta Y.","year":"2003","journal-title":"Plant Biology"},{"key":"e_1_2_11_14_1","doi-asserted-by":"crossref","first-page":"395","DOI":"10.3389\/fpls.2014.00395","article-title":"An Update on Post\u2010Translational Modifications of Hydroxyproline\u2010Rich Glycoproteins: Toward a Model Highlighting Their Contribution to Plant Cell Wall Architecture","volume":"5","author":"Hijazi M.","year":"2014","journal-title":"Frontiers in Plant Science"},{"issue":"5","key":"e_1_2_11_15_1","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1051\/agro:19980505","article-title":"Genetics and Genetic Modifications of Plant Architecture in Grain Legumes: A Review","volume":"18","author":"Huyghe C.","year":"1998","journal-title":"Agronomie"},{"issue":"3","key":"e_1_2_11_16_1","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1007\/BF02859119","article-title":"Taxonomy of the Genus Glycine, Domestication and Uses of Soybeans","volume":"35","author":"Hymowitz T.","year":"1981","journal-title":"Economic Botany"},{"issue":"1","key":"e_1_2_11_17_1","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1186\/s13059-024-03454-w","article-title":"Transcriptional Regulatory Network Reveals Key Transcription Factors for Regulating Agronomic Traits in Soybean","volume":"25","author":"Jiao W.","year":"2024","journal-title":"Genome Biology"},{"issue":"7","key":"e_1_2_11_18_1","doi-asserted-by":"crossref","first-page":"4823","DOI":"10.1111\/pce.15473","article-title":"Exploring Plant Resilience Through Secondary Metabolite Profiling: Advances in Stress Response and Crop Improvement","volume":"48","author":"Khan N.","year":"2025","journal-title":"Plant, Cell & Environment"},{"key":"e_1_2_11_19_1","first-page":"1","volume-title":"Soybean Production Technology: Physiology, Production and Processing","author":"Kumari S.","year":"2025"},{"issue":"3","key":"e_1_2_11_20_1","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1038\/nrg2719","article-title":"Establishing, Maintaining and Modifying DNA Methylation Patterns in Plants and Animals","volume":"11","author":"Law J. A.","year":"2010","journal-title":"Nature Reviews Genetics"},{"issue":"11","key":"e_1_2_11_21_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0026720","article-title":"Archaeological Soybean (Glycine max) in East Asia: Does Size Matter?","volume":"6","author":"Lee G.\u2010A.","year":"2011","journal-title":"PLoS One"},{"key":"e_1_2_11_22_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2024.1477616","article-title":"Molecular and Genetic Basis of Plant Architecture in Soybean","volume":"15","author":"Li W.","year":"2024","journal-title":"Frontiers in Plant Science"},{"issue":"6","key":"e_1_2_11_23_1","doi-asserted-by":"crossref","first-page":"2911","DOI":"10.1111\/brv.12785","article-title":"What Do We Know about Growth of Vessel Elements of Secondary Xylem in Woody Plants?","volume":"96","author":"Miodek A.","year":"2021","journal-title":"Biological Reviews"},{"key":"e_1_2_11_24_1","first-page":"1","volume-title":"Oilseeds: Health Attributes and Food Applications","author":"Modgil R.","year":"2020"},{"issue":"1","key":"e_1_2_11_25_1","doi-asserted-by":"crossref","DOI":"10.64013\/bbasr.v2026i1.124","article-title":"Genome\u2010Wide Identification and Characterization of Plant Specific BPC Transcription Factor Gene Family in Cotton","volume":"2026","author":"Nadeem M.","year":"2026","journal-title":"Bulletin of Biological and Allied Sciences Research"},{"issue":"7","key":"e_1_2_11_26_1","doi-asserted-by":"crossref","first-page":"2534","DOI":"10.1093\/plcell\/koac118","article-title":"Molecular Mechanisms Underlying Leaf Development, Morphological Diversification, and Beyond","volume":"34","author":"Nakayama H.","year":"2022","journal-title":"Plant Cell"},{"key":"e_1_2_11_27_1","doi-asserted-by":"crossref","DOI":"10.1199\/tab.0177","article-title":"Vascular Cambium Development","volume":"13","author":"Nieminen K.","year":"2015","journal-title":"Arabidopsis Book"},{"issue":"19","key":"e_1_2_11_28_1","doi-asserted-by":"crossref","first-page":"2554","DOI":"10.3390\/plants11192554","article-title":"The Anatomical Basis of Heavy Metal Responses in Legumes and Their Impact on Plant\u2013Rhizosphere Interactions","volume":"11","author":"Pandey A. K.","year":"2022","journal-title":"Plants"},{"key":"e_1_2_11_29_1","unstructured":"Petrella R.2020. BASIC PENTACYSTEINE PROTEINs: Understanding Their Roles and Molecular Mechanisms During Reproductive Development in Arabidopsis thaliana."},{"key":"e_1_2_11_30_1","first-page":"3","volume-title":"Soybeans","author":"Ramlal A.","year":"2026"},{"issue":"6","key":"e_1_2_11_31_1","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.3390\/genes14061281","article-title":"Multi\u2010Omics Pipeline and Omics\u2010Integration Approach to Decipher Plant's Abiotic Stress Tolerance Responses","volume":"14","author":"Roychowdhury R.","year":"2023","journal-title":"Genes"},{"issue":"2","key":"e_1_2_11_32_1","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1007\/s00425-023-04188-y","article-title":"Plant BBR\/BPC Transcription Factors: Unlocking Multilayered Regulation in Development, Stress and Immunity","volume":"258","author":"Sahu A.","year":"2023","journal-title":"Planta"},{"key":"e_1_2_11_33_1","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1007\/978-981-97-1699-9_25","volume-title":"Molecular Dynamics of Plant Stress and Its Management","author":"Satrio R. D.","year":"2024"},{"key":"e_1_2_11_34_1","unstructured":"Sharma A.2010. Systematic analysis of Nutritional Components Cell Wall Chemical Features and Potential Pathway (S) of Assimilate Transport in The Developing Pods and Seeds of Medicago truncatula: University of Arkansas at Little Rock."},{"issue":"1","key":"e_1_2_11_35_1","first-page":"9","article-title":"Structure and Function of Plant Cell Wall Proteins","volume":"5","author":"Showalter A. M.","year":"1993","journal-title":"Plant Cell"},{"key":"e_1_2_11_36_1","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1007\/978-981-96-7838-9_13","volume-title":"Fundamentals of Legume Breeding: A Text for Students and Practitioners","author":"Singh K.","year":"2025"},{"issue":"3","key":"e_1_2_11_37_1","doi-asserted-by":"crossref","DOI":"10.1002\/tpg2.20059","article-title":"Genome\u2010Wide Association Analysis of Sucrose Concentration in Soybean (Glycine max L.) Seed Based on High\u2010Throughput Sequencing","volume":"13","author":"Sui M.","year":"2020","journal-title":"Plant Genome"},{"key":"e_1_2_11_38_1","doi-asserted-by":"crossref","first-page":"466","DOI":"10.3389\/fpls.2019.00466","article-title":"Phylogenetic Analyses and GAGA\u2010Motif Binding Studies of Bbr\/Bpc Proteins Lend to Clues in Gaga\u2010Motif Recognition and a Regulatory Role in Brassinosteroid Signaling","volume":"10","author":"Theune M. L.","year":"2019","journal-title":"Frontiers in Plant Science"},{"issue":"21","key":"e_1_2_11_39_1","doi-asserted-by":"crossref","first-page":"3073","DOI":"10.3390\/plants13213073","article-title":"Advances in Soybean Genetic Improvement","volume":"13","author":"Vargas\u2010Almendra A.","year":"2024","journal-title":"Plants"},{"issue":"1","key":"e_1_2_11_40_1","doi-asserted-by":"crossref","first-page":"36","DOI":"10.3390\/genes16010036","article-title":"Genome\u2010Wide Identification, Conservation, and Expression Pattern Analyses of the BBR\u2010BPC Gene Family Under Abiotic Stress in Brassica Napus L","volume":"16","author":"Wang L.","year":"2024","journal-title":"Genes"},{"issue":"6","key":"e_1_2_11_41_1","doi-asserted-by":"crossref","first-page":"1642","DOI":"10.1016\/j.cj.2023.08.002","article-title":"Regulation of Soybean Stem Growth Habit: A Ten\u2010Year Progress Report","volume":"11","author":"Xiong S.\u2010S.","year":"2023","journal-title":"Crop Journal"},{"issue":"1","key":"e_1_2_11_42_1","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1186\/s12870-025-06457-2","article-title":"Integrative QTL Mapping and Candidate Gene Analysis for Main Stem Node Number in Soybean","volume":"25","author":"Zha B.","year":"2025","journal-title":"BMC Plant Biology"},{"issue":"13","key":"e_1_2_11_43_1","doi-asserted-by":"crossref","first-page":"6323","DOI":"10.3390\/ijms26136323","article-title":"Functional Genomics: From Soybean to Legume","volume":"26","author":"Zhou C.","year":"2025","journal-title":"International Journal of Molecular Sciences"}],"container-title":["Plant, Cell &amp; Environment"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/pce.70872","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/pce.70872","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/pce.70872","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T13:50:15Z","timestamp":1789048215000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/pce.70872"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,10]]},"references-count":42,"alternative-id":["10.1111\/pce.70872"],"URL":"https:\/\/doi.org\/10.1111\/pce.70872","archive":["Portico"],"relation":{},"ISSN":["0140-7791","1365-3040"],"issn-type":[{"value":"0140-7791","type":"print"},{"value":"1365-3040","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,10]]},"assertion":[{"value":"2026-06-25","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-09-02","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-09-10","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"pce.70872"}}