Phytoene synthase modulates seed longevity via β-carotene derived metabolites

Seed longevity, the seed's ability to stay viable over time, is an important trait in agriculture that remains a fundamental topic in plant biology. Here, we discovered a function of carotenoid metabolites in prolonging seed lifespan. We found that phytoene synthase (PSY), a major rate-limiting enzyme in carotenoid biosynthesis, modulated seed storability in Arabidopsis (Arabidopsis thaliana) under both natural and artificial aging conditions. Seeds from PSY overexpression lines exhibited significantly enhanced lifespan with low levels of reactive oxygen species (ROS), a major factor affecting longevity. In contrast, seeds from psy mutants had decreased viability with high ROS levels. Both lutein and β-carotene were detected in seeds. However, only β-carotene and its derived apocarotenoids, β-cyclocitral and β-ionone, improved seed lifespan. Seeds from a carotenoid cleavage dioxygenase 1 and 4 (ccd1/4) double mutant and ccd1/4 PSY overexpressing lines had significantly reduced seed longevity, supporting that β-carotene cleavage is necessary for preserving seed lifespan. Comparative proteomic analysis identified TIP2;2, an aquaporin protein, with differential abundances in seeds of PSY overexpression and psy mutant lines. The tip2;2 mutant had reduced seed longevity, and its promoter was transactivated by apocarotenoids. Overexpression of PSY in tip2;2 failed to fully reverse the effects of the mutation, indicating that TIP2;2 is required for the PSY-regulated seed longevity. This study uncovers a role of apocarotenoids in protecting seed longevity and highlights the importance of seed carotenoid production in strengthening agriculture.