Phytoene synthasemodulates seed longevity via the action of β-carotene derived metabolites

Seed longevity, the seed’s ability to stay viable over time, is an important trait in agriculture. Despite extensive research, seed longevity remains one of the fundamental topics in plant biology. Here, we discovered the novel role of carotenoid metabolites in prolonging seed lifespan. We found thatphytoene synthase(PSY), the gene encoding a major rate-limiting enzyme in carotenoid biosynthesis, modulated seed storability in Arabidopsis under both natural and artificial aging conditions. Seeds from thePSYoverexpression (OE) lines exhibited significantly enhanced lifespan with low levels of reactive oxygen species (ROS), a major factor affecting longevity, whereas those from thepsymutants had decreased viability with high ROS levels. While lutein and β-carotene were detected in seeds, only β-carotene and its derived apocarotenoids,i.e.β-cyclocitral and β-ionone, were found to improve seed lifespan. Notably, thecarotenoid cleavage dioxygenase 1and4(ccd1 ccd4) double mutant andPSY ccd1 ccd4seeds showed significantly reduced seed longevity, indicating that β-carotene cleavage is necessary for or it is apocarotenoids playing the role in preserving seed lifespan. Comparative proteomic analysis identified TIP2;2, an aquaporin protein, which showed differential abundances in seeds ofPSYOE andpsymutant vs wild type. The mutanttip2;2had reduced seed longevity, and its promoter was transactivated by apocarotenoids. Collectively, this study uncovers a novel role of apocarotenoids in protecting seed longevity and highlights the importance of seed carotenoid production in strengthening agriculture.