Abstract
Seed development culminates in programmed cell death (PCD) and hardening of organs enclosing the embryo (e.g., pericarp, seed coat) providing essentially a physical shield for protection during storage in the soil. We examined the proposal that dead organs enclosing embryos are unique entities that store and release upon hydration active proteins that might increase seed persistence in soil, germination and seedling establishment. Proteome analyses of dead seed coats of Brassicaceae species revealed hundreds of proteins being stored in the seed coat and released upon hydration, many are stress-associated proteins such as nucleases, proteases and chitinases. Functional analysis revealed that dead seed coats function as long-term storage for multiple active hydrolytic enzymes (e.g., nucleases) that can persist in active forms for decades. Substances released from the dead seed coat of the annual desert plant Anastatica hierochuntica displayed strong antimicrobial activity. Our data highlighted a previously unrecognized feature of dead organs enclosing embryos (e.g., seed coat) functioning not only as a physical shield for embryo protection but also as a long-term storage for active proteins and other substances that are released upon hydration to the “seedsphere” and could contribute to seed persistence in the soil, germination and seedling establishment.
Highlights
The seed coat is a major defense against harmful environmental conditions protecting the embryo from mechanical stress as well as from microorganism invasion and from temperature and humidity fluctuations during storage
To gain insight into proteins released from seeds upon hydration and might contribute to seed germination and seedling establishment, we initially incubated seeds of Arabidopsis thaliana (Col) in phosphate-buffered saline (PBS) buffer at 4 ̊C for 12 h and the supernatant was collected and subjected to proteome analysis using LC-MS/MS followed by identification by Discoverer software against the Uniprot database, which contains plants and fungi proteins; notably, only plant proteins were identified (S1 data)
Implementing the cutoffs we identified 238 proteins that were released from Arabidopsis seeds following hydration (S1 data)
Summary
The seed coat is a major defense against harmful environmental conditions protecting the embryo from mechanical stress as well as from microorganism invasion and from temperature and humidity fluctuations during storage. In Arabidopsis, as well as in other Brassicaceae species, the outer cell layer of the seed coat functions as a special type of secretory cells that synthesize large amounts of pectinaceous mucilage during seed development and maturation [10,11]. This mucilage is rapidly swelled during hydration generating a gelatinous capsule around the seed that functions in seed dispersal and adhesion to soil as well as providing a water reservoir for increasing success of germination, under water scarcity [12,13,14]. Arabidopsis mucilage mutants, including ttg, gl2, atsbt1.7 and dcr-1 germinated normally under non-stressed conditions but displayed reduced germination and seedling establishment in the presence of polyethylene glycol [17,18,19]
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