Germination sensu stricto in Arabidopsis involves seed coat and endosperm rupture by the emerging seedling root. Subsequently the cotyledons emerge rapidly from the extraembryonic tissues of the seed, allowing autotrophic seedling establishment. Seedling survival depends upon the presence of an intact seedling cuticle that prevents dehydration, and which has hitherto been assumed to form the interface between the newly germinated seedling and its environment. Here we show that in Arabidopsis this is not the case. The primary interface between the emerging seedling and its environment is formed by an extra-cuticular endosperm-derived glycoprotein-rich structure called the sheath, which is maintained as a continuous layer at seedling surfaces during germination, and becomes fragmented as cotyledons expand. Mutants lacking an endosperm specific cysteine-rich peptide (KERBEROS (KRS)), show a complete loss of sheath production. Although krs mutants have no defects in germination sensu stricto they show a delay in cotyledon emergence, a defect not observed in seedlings with defects in cuticle biosynthesis. Biophysical analyses reveal that the surfaces of wild-type cotyledons show minimal adhesion to silica beads in an aqueous environment at cotyledon emergence, but that adhesion increases as cotyledons expand. In contrast krs mutant cotyledons show enhanced adhesion at germination. Mutants with defects in cuticle biosynthesis, but no sheath defects, show a similar adhesion profile to wild-type seedlings at germination. We propose that the sheath reduces the adhesiveness of the cotyledon surface under the humid conditions necessary for seed germination, and thus promotes seed coat shedding and rapid seedling establishment.

The cuticle is the plant’s outermost layer that covers the surfaces of aerial parts. This structure is composed of a variety of aliphatic molecules and is well-known for its protective role against biotic and abiotic stresses in plants. Mutants with a permeable cuticle show developmental defects such as organ fusions and altered seed germination and viability. In this study, we identified a novel maize mutant, stocky1, with unique features: lethal at the seedling stage, and showing a severely dwarfed phenotype, due to a defective cuticle. For the first time, the mutant was tentatively mapped to chromosome 5, bin 5.04. The mutant phenotype investigated in this work has the potential to contribute to the elucidation of the role of the cuticle during plant development. The possibility of controlling this trait is of relevance in the context of climate change, as it may contribute to tolerance to abiotic stresses.