An Improved Genome-Wide Association Procedure Explores Gene–Allele Constitutions and Evolutionary Drives of Growth Period Traits in the Global Soybean Germplasm Population

In soybeans (Glycine max (L.) Merr.), their growth periods, DSF (days of sowing-to-flowering), and DFM (days of flowering-to-maturity) are determined by their required accumulative day-length (ADL) and active temperature (AAT). A sample of 354 soybean varieties from five world eco-regions was tested in four seasons in Nanjing, China. The ADL and AAT of DSF and DFM were calculated from daily day-lengths and temperatures provided by the Nanjing Meteorological Bureau. The improved restricted two-stage multi-locus genome-wide association study using gene–allele sequences as markers (coded GASM-RTM-GWAS) was performed. (i) For DSF and its related ADL(DSF) and AAT(DSF), 130–141 genes with 384–406 alleles were explored, and for DFM and its related ADL(DFM) and AAT(DFM), 124–135 genes with 362–384 alleles were explored, in a total of six gene–allele systems. DSF shared more ADL and AAT contributions than DFM. (ii) Comparisons between the eco-region gene–allele submatrices indicated that the genetic adaptation from the origin to the geographic sub-regions was characterized by allele emergence (mutation), while genetic expansion from primary maturity group (MG)-sets to early/late MG-sets featured allele exclusion (selection) without allele emergence in addition to inheritance (migration). (iii) Optimal crosses with transgressive segregations in both directions were predicted and recommended for breeding purposes, indicating that allele recombination in soybean is an important evolutionary drive. (iv) Genes of the six traits were mostly trait-specific involved in four categories of 10 groups of biological functions. GASM-RTM-GWAS showed potential in detecting directly causal genes with their alleles, identifying differential trait evolutionary drives, predicting recombination breeding potentials, and revealing population gene networks.