Research Article: The dead seed coat functions as a long-term storage for active hydrolytic enzymes

Date Published: July 11, 2017

Publisher: Public Library of Science

Author(s): Buzi Raviv, Lusine Aghajanyan, Gila Granot, Vardit Makover, Omer Frenkel, Yitzchak Gutterman, Gideon Grafi, Belay T. Ayele.

http://doi.org/10.1371/journal.pone.0181102

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.

Partial Text

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. The seed coat is of maternal origin and is derived from the integuments (inner and outer) surrounding the ovule. However, it is not clear whether the dead seed coat was evolved to provide just a passive, physical shield for embryo protection or may represent also an active entity that stores and releases upon hydration substances (proteins, metabolites) that aid in seed persistence and longevity, germination and seedling establishment.

The seed coat and other hardened parts enclosing the embryo are commonly considered as a passive barrier protecting the embryo from harmful environmental conditions. Here we showed that the dead organ enclosing embryos functions as a storage for active hydrolases and antimicrobial substances that might play important role in regulating seed longevity, germination and seedling establishment. Indeed, the seed coat has been implicated in dormancy and seed longevity and quality [52] and some reports have also suggested the function of the seed coat in storing antimicrobial substances such as tannins, flavonoids and anti fungal proteins that may protect the embryo and germinating seeds from pathogens [27,53].

The finding that proteins are stored and remained active within essentially dead organs of the seed coat for many years is puzzling. It is commonly believed that cellular proteins undergo complete degradation when cell die and their constituents are remobilized to other parts of the plants (young leaves, fruits, embryos). Based on the data presented here and in other report [31] we suggest that seed coat and also other dead hardened parts enclosing embryos (e.g., glumes, lemmas and palease in Poaceae species, [31]) were evolved not just for providing a physical shield for embryo protection but also as storage organs for multiple active proteins and probably metabolites and other substances for the purpose of nourishment as well as protection of germinating seeds from soil pathogens, which may facilitate seed persistence in the soil, germination and seedling establishment in wild as well as in agroecosystem [76].

 

Source:

http://doi.org/10.1371/journal.pone.0181102

 

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