A polygalacturonase gene PG031 regulates seed coat permeability with a pleiotropic effect on seed weight in soybean.

KEY MESSAGE: A QTL gene PG031 regulates the seed coat permeability and seed weight. The critical SNP that can explain the variation of permeability in soybean population can be used for seed improvement. Seed coat permeability is a critical trait for soybean and is tightly associated with seed storage longevity, germination, soy-food processing, and other commercially important traits. However, the molecular mechanism of such an important trait in soybean is largely unclear. In the present study, we uncovered a polygalacturonase (PG) gene, PG031, which controls seed coat permeability in soybean. PG031 exhibited tissue expression specificity in flowers while it was strongly induced in the seed coat and radical upon imbibition. Subcellular localization localized PG031 to the cell wall, suggesting its role specific to the cell wall of the seed coat. Natural variation analysis reveals three haplotypes (PG031289H, PG031289Y, and PG031Hap3) and the single nucleotide polymorphism (SNP) variation for H289Y may explain the variation in permeability in cultivated soybean population. Overexpression of impermeable allele PG031289H significantly reduced the seed coat permeability and 100-seed weight in transgenic seeds through decreasing intracellular spaces of the osteosclereid layer and parenchyma of the seed coat to decline water accessing the seed. PG031 was also located within a quantitative trait locus (QTL) explaining ~ 15% of total phenotypic variation in permeability, nominating it the QTL gene controlling permeability. PG031289Y allele associated with high permeability and high seed weight is experiencing ongoing artificial selection. The results provide insight into the genetic mechanism of seed coat permeability and indicate its potential for the improvement of permeability-associated seed traits in soybean.