Fruit Spray of 24-Epibrassinolide and Fruit Shade Alter Pericarp Photosynthesis Activity and Seed Lipid Accumulation in Styrax tonkinensis

As demand for biofuel feedstock production increases, the substitutable woody oilseed benzoin (Styrax tonkinensis (Pierre) Craib ex Hartwich) has received increased attention among Chinese researchers. However, the mechanism of seed oil regulation has not been revealed in this species. Maternal control of seed lipid content has been observed in many plant species. In this study, in planta treatments were applied to create different pericarp photosynthesis activation levels in benzoin. Compared with fruit shading treatment, superior photosynthetic physiological characteristics were found in the brassinosteroid hormone 24-epibrassinolide-treated pericarps during maturation (56–112 days after flowering); specifically, these superior characteristics were reflected by higher average and peak values of the Chl a/b ratio, NADPH/NADP+ ratio, NADP-dependent malate dehydrogenase activity, and ribulose 1,5-bisphosphate carboxylase/oxygenase activity. Next, we found that the pericarp-encapsulated seed yield and oil content were closely connected to the maternal-specific photosynthetic events. The enhanced pericarp photosynthesis activity (treated with 10 μM brassinosteroid) was accompanied by higher fatty acid synthase activity and a faster lipid deposition rate, which was verified by transmission electron microscopy. These changes led to a final increase in the total fatty acid (FA) content of mature seeds of 19%, which could be largely accounted for by the elevated saturated FA (mostly long-chain FAs) percentage in benzoin oil. When benzoin fruits grew in low light (bagged in three layers of black non-woven fabrics), lipid synthesis capability was markedly impaired. The dynamics of cellular storage reserves were further analyzed, suggesting that the pericarp-seed carbohydrate translocation efficiency in fruits and the carbon partitioning among seed reserves were directly responsible for the seed oil diversification under the treatments. Taken together, our results highlighted the maternal control, via pericarp photosynthesis, over the regulation of the seed oil content in benzoin.