Embryonal degreening and seed longevity require plastid LEA proteins

Seeds enable plant embryos to endure extended periods and environmental extremes. Orthodox seeds acquire desiccation tolerance during maturation, before metabolic quiescence. Coordinated thylakoid disassembly and Chl degradation lead to embryo degreening, a hallmark of orthodox seed maturation. While degreening is hormonally controlled, our understanding of the molecular players involved and its physiological significance remains incomplete. By serendipity, we observed a stay-green seed phenotype in an Arabidopsis thaliana mutant lacking two LATE EMBRYOGENESIS ABUNDANT (LEA) proteins, LEA42 and LEA48, which we identified as the most abundant LEA proteins in seed mitochondria and plastids. Using lea48xlea42 as a model for impaired LEA function in seed mitochondria and plastids, proteomic, transcriptomic and transmission electron microscopy analyses indicate incomplete thylakoid degradation. Freshly harvested lea48xlea42 seeds were unaffected in germination but were impaired in germination after high-temperature/high-humidity ageing. Genetic complementation with specifically targeted LEA expression in either mitochondria or chloroplasts revealed that seed longevity support is associated with plastidial, but not mitochondrial, LEA. Light exposure of mature seeds ('light storage') reduced longevity, providing a physiological framework for embryo degreening. Our data identify a role for LEA proteins in remodelling seed plastids before maturation drying and highlight LEA-dependent embryo degreening as a decisive contributor to seed longevity.