Tree peony transcription factor PrRAP2.1 promotes seed oil accumulation

Tree peony ( Paeonia rockii ) is a promising woody oilseed crop valued for its seed oil, which is rich in abundant unsaturated fatty acids beneficial to human health. However, the transcription factors (TFs) responsible for high-quality oil accumulation in tree peony remain largely unexplored. Here, integrated histological and transcriptomic analyses of P. rockii seeds revealed a vital role for ERF TFs in seed development and oil accumulation. Characterization and expression profiling of 12 ERF genes identified PrRAP2.1 , which is predominantly expressed in developing seeds and functions as a key positive regulator of seed oil accumulation. Our results show that PrRAP2.1 displays a specific, endosperm-predominant, development-dependent expression pattern and encodes a protein localized in the nucleus. Overexpression of PrRAP2.1 in Arabidopsis significantly promoted seed development, and regulated oil accumulation by increasing the content of the triacylglycerol (TAG) precursor diacylglycerol (DAG), thereby enhancing the total seed oil content by up to 5.57 %; Furthermore, it improved the fatty acid composition by elevating the substrate PC (18:2/18:2) pool, resulting in an increased C18:2-PC/C18:3-PC ratio and a significant accumulation of C18:2. Collectively, these findings provide novel insights into the role of PrRAP2.1 in promoting seed oil accumulation and lay the groundwork for enhancing oil yield in tree peony and other oilseed crops. Seed oils serve as an essential energy reserve for plant growth, a vital component of human nutrition, and a valuable raw material for diverse industrial applications. In this study, we integrated WGCNA with expression profiling to identify ERF transcription factors strongly associated with seed oil biosynthesis in tree peony. Subsequent characterization and expression analysis revealed a gene, PrRAP2.1 , which encodes a nuclear-localized protein. Heterologous expression of PrRAP2.1 in Arabidopsis substantially increased seed oil content. • Twelve ERFs genes highly associated with seed oil synthesis were identified in the Paeonia rockii genome. • PrRAP2.1 exhibits endosperm-specific and spatiotemporal expression patterns in plant seeds, and is differentially expressed in high-oil-content germplasms. • Whole-gene and segmental duplications contributed to the expansion of PrERF s family. • PrRAP2.1 encodes a nuclear-localized protein. • PrRAP2.1 enhances seed oil accumulation by positively regulating the levels of DAG and C18:2-PC.