Metabolic switching of astringent and beneficial triterpenoid saponins in soybean is achieved by a loss-of-function mutation in cytochrome P450 72A69

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Triterpenoid saponins are major components of secondary metabolites in soybean seeds and are divided into two groups: group A saponins, and 2,3-dihydro-2,5-dihydroxy-6-methyl-4H-pyran-4-one (DDMP) saponins. The aglycone moiety of group A saponins consists of soyasapogenol A (SA), which is an oxidized β-amyrin product, and the aglycone moiety of the DDMP saponins consists of soyasapogenol B (SB). Group A saponins produce a bitter and astringent aftertaste in soy products, whereas DDMP saponins have known health benefits for humans. We completed map-based cloning and characterization of the geneSg-5, which is responsible for SA biosynthesis. The naturally occurringsg-5mutant lacks group A saponins and has a loss-of-function mutation (L164*) inGlyma15g39090, which encodes the cytochrome P450 enzyme, CYP72A69. An enzyme assay indicated the hydroxylase activity of recombinant CYP72A69 against SB, which also suggested the production of SA. Additionally, inducedGlyma15g39090mutants (R44* or S348P) lacked group A saponins similar to thesg-5mutant, indicating thatGlyma15g39090corresponds toSg-5. Endogenous levels of DDMP saponins were higher in thesg-5mutant than in the wild-type lines due to the loss of the enzyme activity that converts SB to SA. Interestingly, the genomes of palaeopolyploid soybean and the closely related common bean carry multipleSg-5paralogs in a genomic region syntenic to the soybeanSg-5region. However, SA did not accumulate in common bean samples, suggesting that Sg-5 activity evolved after gene duplication event(s). Our results demonstrate that metabolic switching of undesirable saponins with beneficial saponins can be achieved in soybean by disablingSg-5.

Significance Statement

Triterpenoid saponins in soybeans are divided into two groups: bitter and astringent group A saponins, and health-promoting DDMP saponins. Disabling a single cytochrome P450 gene (Sg-5) can switch the metabolism from the undesirable group A saponins to the beneficial DDMP saponins. This finding will help soybean breeders improve the quality and consumer acceptance of soy food products.

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