TaNF-Y-PRC2 orchestrates temporal control of starch and protein synthesis in wheat

The endosperm in cereal grains is instrumental in determining grain yield and seed quality, as it controls the production of starch and protein. In this study, we identified a specific TaNF-Y trimeric complex, consisting of TaNF-YA3-D, TaNF-YB7-B, and TaNF-YC6-B, exhibiting robust expression within endosperm during grain filling stage in wheat. Knock-down of either TaNF-YA3 or TaNF-YC6 led to less starch but more gluten proteins. Detailed analyses have unveiled that the TaNF-Y indirectly boosts starch biosynthesis genes by reducing TaNAC019, a repressor of TaAGPS1a, TaSuS2, thereby regulating starch biosynthesis. Conversely, the TaNF-Y directly inhibits the expression of gliadin and low molecular weight (LMW)-GS coding genes, including TaGli-{gamma}-700 and TaLMW-400. Furthermore, the TaNF-Y components interact with TaSWN, the histone methyltransferase subunit of Polycomb repressive complex 2 (PRC2), to repress the expression of TaNAC019, TaGli-{gamma}-700, and TaLMW-400 through H3K27me3 modification. Notably, weak mutation of TaFIE, core subunit of PRC2, has reduced starch but elevated gliadin and LMW-GS levels. Intriguingly, DNA variations of TaNF-Y components are widely associated with seed developmental traits. In particular, variation within the coding region of TaNF-YB7-B is linked to differences in starch and protein content. Distinct haplotypes of TaNF-YB7-B affect its interaction with TaSWN, influencing the repression of targets like TaNAC019 and TaGli-{gamma}-700. Our findings illuminate the intricate molecular mechanisms governing epigenetic regulation by the TaNF-Y-PRC2 for wheat endosperm development. Manipulating the TaNF-Y complex holds potential for optimizing grain yield and enhancing quality.