In many higher plants, seed oil accumulation is governed by complex multilevel regulatory networks including transcriptional regulation, which primarily affects fatty acid biosynthesis. Tree peony (Paeonia rockii), a perennial deciduous shrub endemic to China is notable for its seed oil that is abundant in unsaturated fatty acids. We discovered that a tree peony trihelix transcription factor, PrASIL1, localized in the nucleus, is expressed predominantly in developing seeds during maturation. Ectopic overexpression of PrASIL1 in Nicotiana benthamiana leaf tissue and Arabidopsis thaliana seeds significantly reduced total fatty acids and altered the fatty acid composition. These changes were in turn associated with the decreased expression of multitudinous genes involved in plastidial fatty acid synthesis and oil accumulation. Thus, we inferred that PrASIL1 is a critical transcription factor that represses oil accumulation by down-regulating numerous key genes during seed oil biosynthesis. In contrary, up-regulation of oil biosynthesis genes and a significant increase in total lipids and several major fatty acids were observed in PrASIL1-silenced tree peony leaves. Together, these results provide insights into the role of trihelix transcription factor PrASIL1 in controlling seed oil accumulation. PrASIL1 can be targeted potentially for oil enhancement in tree peony and other crops through gene manipulation.

Tree peony is a perennial deciduous shrub with great ornamental and medicinal value. A limitation of its current functional genomic research is the lack of effective molecular genetic tools. Here, the first application of a Tobacco rattle virus (TRV)-based virus-induced gene silencing (VIGS) in the tree peony species Paeonia ostii is presented. Two different approaches, leaf syringe-infiltration and seedling vacuum-infiltration, were utilized for Agrobacterium-mediated inoculation. The vacuum-infiltration was shown to result in a more complete Agrobacterium penetration than syringe-infiltration, and thereby determined as an appropriate inoculation method. The silencing of reporter gene PoPDS encoding phytoene desaturase was achieved in TRV-PoPDS-infected triennial tree peony plantlets, with a typical photobleaching phenotype shown in uppermost newly-sprouted leaves. The endogenous PoPDS transcripts were remarkably down-regulated in VIGS photobleached leaves. Moreover, the green fluorescent protein (GFP) fluorescence was detected in leaves and roots of plants inoculated with TRV-GFP, suggesting the capability of TRV to silence genes in various tissues. Taken together, the data demonstrated that the TRV-based VIGS technique could be adapted for high-throughput functional characterization of genes in tree peony.

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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.

Tree peonies (Paeonia Section Moutan)—including nine wild species, which belong to subsections Vaginatae and Delavayanae—are economically important plants with ornamental, nutritional, and medicinal applications. In this study, for the first time, we determined the bioactive components and antioxidant activities and antibacterial activities of the newly grown leaves of nine wild tree peony species (WTPS). A total of 276 bioactive components were identified through non-targeted metabolomics; more than 80% of the 276 metabolites identified are terpenoids and flavonoids. A total of 42 differential metabolites were quantitatively determined. The main differential metabolites were Paeoniflorin, Luteoloside, Hyperin, Apigenin-7-glucoside, Rhoifolin, and Cantharidin. Such a high terpenoid and flavonoid content of the leaf extracts renders them as species with strong antibacterial capacities, and most of the bacteria tested showed greater sensitivity derived from the members of subsection Vaginatae than those of subsection Delavayanae. All WTPS have significant antioxidant activity; this activity is attributed to high levels of the total phenolic content (TPC) and total flavonoid content (TFC), of which, among the nine WTPS, P. lutea has the strongest antioxidant capacity. Our results provided a theoretical basis for the in-deep application of tree peony leaves for food, medical, and pharmaceutical industries.