Endosperm-specific expressed transcription factor protein WRINKLED1-mediated oil accumulative mechanism in woody oil peony Paeonia ostii var. lishizhenii

Paeonia ostii var. lishizhenii exhibits superiority of high α-linolenic acid in seed oils, yet, the low yield highlights the importance of enhancing oil accumulation in seeds for edible oil production. The transcription factor protein WRINKLED1 (WRI1) plays crucial roles in modulating oil content in higher plants; however, its functional characterization remains elusive in P. ostii var. lishizhenii. Herein, based on a correlation analysis of transcription factor transcript levels, FA accumulation rates, and interaction assay of FA biosynthesis associated proteins, a WRI1 homologous gene (PoWRI1) that potentially regulated oil content in P. ostii var. lishizhenii seeds was screened. The PoWRI1 exhibited an endosperm-specific and development-depended expression pattern, encoding a nuclear-localized protein with transcriptional activation capability. Notably, overexpressing PoWRI1 upregulated certain key genes relevant to glycolysis, FA biosynthesis and desaturation, and improved seed development, oil body formation and oil accumulation in Arabidopsis seeds, resulting an enhancement of total seed oil weight by 9.47–18.77 %. The defective impacts on seed phenotypes were rescued through ectopic induction of PoWRI1 in wri1 mutants. Our findings highlight the pivotal role of PoWRI1 in controlling oil accumulation in P. ostii var. lishizhenii, offering bioengineering strategies to increase seed oil accumulation and enhance its potential for edible oil production. •PoWRI1 is a key regulator controlling oil accumulation in Paeonia ostii endosperms.•The expression pattern of PoWRI1 is dependent on endosperm development.•PoWRI1 improves seed development, oil body formation and FA synthesis in Arabidopsis.•PoWRI1 modulates FA composition and related gene expression in Arabidopsis seeds.•PoWRI1 rescues the defective impacts caused by loss function of AtWRI1 in wri1 mutants.