The tree peony nuclear factor Y transcription factor PrNF‐YC2 promotes seed oil accumulation.

SUMMARY: Seed oil not only provides energy for seed postgermination development but also provides essential nutrients and raw materials for human products. However, the transcriptional regulatory mechanism controlling seed oil accumulation remains largely unknown. Tree peony (Paeonia rockii) is an emerging woody oilseed crop in China that is known for its high‐quality seed oil. Here, we revealed that a tree peony nuclear factor Y transcription factor, PrNF‐YC2, is expressed predominantly in developing seeds and functions as an essential positive regulator of seed oil accumulation. PrNF‐YC2 promoted oil accumulation in both transient ectopic overexpression Nicotiana benthamiana leaves and stable transgenic Arabidopsis thaliana seeds, globally upregulating the expression of genes involved in oil accumulation. In contrast, PrNF‐YC2‐silenced tree peony leaves using a virus‐induced gene silencing system showed reduced oil content and expression of oil synthesis‐related genes, including four master positive regulators contributing to oil accumulation, namely, LEAFY COTYLEDON1 (LEC1), ABSCISIC ACID INSENSITIVE3 (ABI3), FUSCA3 (FUS3), and WRINKLED1 (WRI1). We demonstrated that PrNF‐YC2 directly activates PrLEC1 and PrABI3 alone and indirectly activates PrFUS3 and PrWRI1 by interacting with PrLEC1. Moreover, interaction with PrLEC1 also enhances the activation capacity of PrNF‐YC2. The activation of these four master positive regulators by PrNF‐YC2 triggered the upregulation of numerous oil synthesis‐related genes, thus promoting oil accumulation. These findings provide new insights into the regulatory mechanism of seed oil accumulation and manipulation of PrNF‐YC2 may be beneficial for enhancing oil yield in tree peony and other oilseed crops. Significance Statement: We show that the tree peony NF‐Y transcriptional factor PrNF‐YC2 directly activates PrLEC1 and PrABI3 alone and indirectly activates PrFUS3 and PrWRI1 by recruiting PrLEC1, thus plays an essential role in seed oil accumulation. To our knowledge, this study demonstrates for the first time that NF‐YC transcription factor is a major gene that regulates seed oil accumulation via dual modes. This study also enriches our knowledge of the transcriptional regulation of LEC1. [ABSTRACT FROM AUTHOR]