Genetic architecture of condensed tannins accumulated in wheat grains

Wheat grains contain various bioactive substances, of which, condensed tannins (CT) are polymeric flavan-3-ols that accumulate in wheat seed coat influencing the end-use quality and nutritional value. However, the genetic architecture underlying CT biosynthesis in wheat grain remains unclear. Here, we studied the deposition and genetic regulation of CT in wheat grains, and found that CT deposited specifically in the testa layer of red-grained wheat as catechin- and epicatechin-formed polymers. Genome-wide association study identified 22 genetic loci affecting CT content, one of which, TaTAN, a single dominant gene controlling CT presence, was mapped to chromosome 3A in a segregation population. Further pan-genome analysis, transcriptome profiling and ethyl methanesulfonate induced mutants sequencing revealed a R2R3-MYB transcription factor, TaMYB10-3A, as the causal gene. Three loss-of-function alleles in TaMYB10-3A caused by large fragment inversion-deletion and insertion were identified which abolish both CT deposition and red pigmentation, demonstrating the pleiotropic effect of TaMYB10-3A on CT presence and grain color. TaMYB10-3A directly trans-activates core flavonoid genes such as chalcone synthase and dihydroflavonol 4-reductase to initiate CT biosynthesis. Our investigation provides a comprehensive understanding of CT presence in wheat grains and lays a solid foundation for manipulating CT metabolites to improve wheat grain end-use quality and nutrition values in wheat.