Artificial selection of mutations in two nearby genes gave rise to shattering resistance in soybean

Resistance to pod shattering is a key domestication-related trait selected for seed production in many crops. Here, we show that the transition from shattering in wild soybeans to shattering resistance in cultivated soybeans resulted from selection of mutations within the coding sequences of two nearby genes - Sh1 and Pdh1. Sh1 encodes a C2H2-like zinc finger transcription factor that promotes shattering by repressing SHAT1-5 expression, thereby reducing the secondary wall thickness of fiber cap cells in the abscission layers of pod sutures, while Pdh1 encodes a dirigent protein that orchestrates asymmetric lignin distribution in inner sclerenchyma, creating torsion in pod walls that facilitates shattering. Integration analyses of quantitative trait locus mapping, genome-wide association studies, and allele distribution in representative soybean germplasm suggest that these two genes are primary modulators underlying this domestication trait. Our study thus provides comprehensive understanding regarding the genetic, molecular, and cellular bases of shattering resistance in soybeans.