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Abstract Background The yield and quality of soybean oil are determined by seed oil-related traits, and metabolites/lipids act as bridges between genes and traits. Although there are many studies on the mode of inheritance of metabolites or traits, studies on multi-dimensional genetic network (MDGN) are limited. Results In this study, six seed oil-related traits, 59 metabolites, and 107 lipids in 398 recombinant inbred lines, along with their candidate genes and miRNAs, were used to construct an MDGN in soybean. Around 175 quantitative trait loci (QTLs), 36 QTL-by-environment interactions, and 302 metabolic QTL clusters, 70 and 181 candidate genes, including 46 and 70 known homologs, were previously reported to be associated with the traits and metabolites, respectively. Gene regulatory networks were constructed using co-expression, protein–protein interaction, and transcription factor binding site and miRNA target predictions between candidate genes and 26 key miRNAs. Using modern statistical methods, 463 metabolite–lipid, 62 trait–metabolite, and 89 trait–lipid associations were found to be significant. Integrating these associations into the above networks, an MDGN was constructed, and 128 sub-networks were extracted. Among these sub-networks, the gene–trait or gene–metabolite relationships in 38 sub-networks were in agreement with previous studies, e.g., oleic acid (trait)–GmSEI–GmDGAT1a–triacylglycerol (16:0/18:2/18:3), gene and metabolite in each of 64 sub-networks were predicted to be in the same pathway, e.g., oleic acid (trait)–GmPHS–d-glucose, and others were new, e.g., triacylglycerol (16:0/18:1/18:2)–GmbZIP123–GmHD-ZIPIII-10–miR166s–oil content. Conclusions This study showed the advantages of MGDN in dissecting the genetic relationships between complex traits and metabolites. Using sub-networks in MGDN, 3D genetic sub-networks including pyruvate/threonine/citric acid revealed genetic relationships between carbohydrates, oil, and protein content, and 4D genetic sub-networks including PLDs revealed the relationships between oil-related traits and phospholipid metabolism likely influenced by the environment. This study will be helpful in soybean quality improvement and molecular biological research.

Introduction: Although seed oil content and its fatty acid compositions in soybean were affected by environment, QTN-by-environment (QEIs) and gene-by-environment interactions (GEIs) were rarely reported in genomewide association studies. Methods: The 3VmrMLM method was used to associate the trait phenotypes, measured in five to seven environments, of 286 soybean accessions with 106,013 SNPs for detecting QTNs and QEIs. Results: Seven oil metabolism genes (GmSACPD-A, GmSACPD-B, GmbZIP123, GmSWEET39, GmFATB1A, GmDGAT2D, and GmDGAT1B) around 598 QTNs and one oil metabolism gene GmFATB2B around 54 QEIs were verified in previous studies; 76 candidate genes and 66 candidate GEIs were predicted to be associated with these traits, in which 5 genes around QEIs were verified in other species to participate in oil metabolism, and had differential expression across environments. These genes were found to be related to soybean seed oil content in haplotype analysis. In addition, most candidate GEIs were co-expressed with drought response genes in co-expression network, and three KEGG pathways which respond to drought were enriched under drought stress rather than control condition; six candidate genes were hub genes in the co-expression networks under drought stress. Discussion: The above results indicated that GEIs, together with drought response genes in co-expression network, may respond to drought, and play important roles in regulating seed oil-related traits together with oil metabolism genes. These results provide important information for genetic basis, molecular mechanisms, and soybean breeding for seed oil-related traits. [ABSTRACT FROM AUTHOR]