Extreme drought alters progeny dispersal unit properties of winter wild oat (Avena sterilis L.).

MAIN CONCLUSION: The dead husk is a vital component of the dispersal unit whose biochemical properties can be modified following exposure to drought. This might affect seed performance and fate, soil properties and consequently plant biodiversity. We investigated the effects of extreme drought on the dispersal unit (DU) properties of winter wild oat (Avena sterilis L.) in the Mediterranean ecosystems focusing on a commonly ignored component of the DU, namely the dead floral bracts (husk). DUs were collected from a climate change experimental research station in the Judean Hills, Israel, simulating extreme drought and from two additional sites differing in the rainfall amounts. Our results showed that drought conditions significantly affected A. sterilis reproductive traits displaying reduced DUs and caryopses weights. The husk contributes profoundly to seed performance showing that germination from the intact DUs or the intact florets 1 was higher, faster and more homogenous compared to naked caryopses; no effect of drought on germination properties was observed. The husk stored hundreds of proteins that retain enzymatic activity and multiple metabolites including phytohormones. Changes in rainfall amounts affected the composition and levels of proteins and other metabolites accumulated in the husk, with a notable effect on abscisic acid (ABA). The husk of both control and drought plants released upon hydration substances that selectively inhibited other species seed germination as well as substances that promoted microbial growth. Our data showed that the dead husk represents a functional component of the DU that have been evolved to nurture the embryo and to ensure its success in its unique habitat. Furthermore, drought conditions can modify husk biochemical properties, which in turn might affect seed performance and fate, soil microbiota and soil fertility and consequently plant species diversity.

Maternal environment alters dead pericarp biochemical properties of the desert annual plant Anastatica hierochuntica L.

The dead organs enclosing embryos (DOEEs) emerge as central components of the dispersal unit (DU) capable for long-term storage of active proteins and other substances that affect seed performance and fate. We studied the effect of maternal environment (salt and salt+heat) on progeny DU (dry indehiscent fruit) focusing on pericarp properties of Anastatica hierochuntica. Stressed plants displayed increased seed abortion and low level and rate of germination. Hydrated pericarps released antimicrobial factors and allelopathic substances that inhibit germination of heterologous species. Proteome analysis of dead pericarps revealed hundreds of proteins, among them nucleases, chitinases and proteins involved in reactive oxygen species detoxification and cell wall modification. Salt treatment altered the composition and level of proteins stored in the pericarp. We observed changes in protein profile released from seeds of salt-treated plants with a notable increase in a small anti-fungal protein, defensin. The levels of phytohormones including IAA, ABA and salicylic acid were reduced in dead pericarps of stressed plants. The data presented here highlighted the predominant effects of maternal environment on progeny DUs of the desert plant A. hierochuntica, particularly on pericarp properties, which in turn might affect seed performance and fate, soil fertility and consequently plant biodiversity.

The Dead Can Nurture: Novel Insights into the Function of Dead Organs Enclosing Embryos.

Plants have evolved a variety of dispersal units whereby the embryo is enclosed by various dead protective layers derived from maternal organs of the reproductive system including seed coats (integuments), pericarps (ovary wall, e.g., indehiscent dry fruits) as well as floral bracts (e.g., glumes) in grasses. Commonly, dead organs enclosing embryos (DOEEs) are assumed to provide a physical shield for embryo protection and means for dispersal in the ecosystem. In this review article, we highlight recent studies showing that DOEEs of various species across families also have the capability for long-term storage of various substances including active proteins (hydrolases and ROS detoxifying enzymes), nutrients and metabolites that have the potential to support the embryo during storage in the soil and assist in germination and seedling establishment. We discuss a possible role for DOEEs as natural coatings capable of "engineering" the seed microenvironment for the benefit of the embryo, the seedling and the growing plant.

Dead Pericarps of Dry Fruits Function as Long-Term Storage for Active Hydrolytic Enzymes and Other Substances That Affect Germination and Microbial Growth.

It is commonly assumed that dead pericarps of dry indehiscent fruits have evolved to provide an additional physical layer for embryo protection and as a means for long distance dispersal. The pericarps of dry fruits undergo programmed cell death (PCD) during maturation whereby most macromolecules such DNA, RNA, and proteins are thought to be degraded and their constituents remobilized to filial tissues such as embryo and endosperm. We wanted to test the hypothesis that the dead pericarp represents an elaborated layer that is capable of storing active proteins and other substances for increasing survival rate of germinating seeds. Using in gel assays we found that dead pericarps of both dehiscent and indehiscent dry fruits of various plant species including Arabidopsis thaliana and Sinapis alba release upon hydration multiple active hydrolytic enzymes that can persist in an active form for decades, including nucleases, proteases, and chitinases. Proteomic analysis of indehiscent pericarp of S. alba revealed multiple proteins released upon hydration, among them proteases and chitinases, as well as proteins involved in reactive oxygen species (ROS) detoxification and cell wall modification. Pericarps appear to function also as a nutritional element-rich storage for nitrate, potassium, phosphorus, sulfur, and others. Sinapis alba dehiscent and indehiscent pericarps possess germination inhibitory substances as well as substances that promote microbial growth. Collectively, our study explored previously unknown features of the dead pericarp acting also as a reservoir of biological active proteins, and other substances capable of "engineering" the microenvironment for the benefit of the embryo.

The dead seed coat functions as a long-term storage for active hydrolytic enzymes.

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.

The dead, hardened floral bracts of dispersal units of wild wheat function as storage for active hydrolases and in enhancing seedling vigor.

It is commonly assumed that the dead, hardened floral bracts of the dispersal unit of grasses have been evolved to protect seeds from predation and / or assist in fruit/caryopsis dispersal. While these structures have important agronomical and economical implications, their adaptive value has not been fully explored. We investigated the hypothesis that the maternally derived hardened floral bracts have been evolved not just as a means for caryopsis protection and dispersal, but also as storage for substances that might affect seed germination and seedling vigor. Dead glumes as well as lemmas and paleas of wild emmer wheat (Triticum turgidum var dicoccoides) were found to store and release upon hydration active hydrolases including nucleases and chitinases. High nuclease activity was released upon hydration from glumes derived from wild strains of wheat including Triticum urartu and wild emmer wheat, while very low nuclease activity was detected in glumes derived from domesticated, free-threshing wheat cultivars (e.g., durum wheat). Germination from the intact dispersal unit of wild emmer wheat was delayed, but post germination growth was better than those of separated caryopses. Most notable was a significant increase in lateral root production on seedlings germinated from the intact dispersal unit. Proteome analysis of wild emmer wheat glumes revealed many proteins stored and released upon hydration including S1-type nucleases, peptidases, antifungal hydrolases such as chitinases and ß-1,3-glucanase as well as pectin acetylesterase, a protein involved in cell wall degradation and remodeling. Also, reactive oxygen species (ROS)-detoxifying enzymes such as superoxide dismutase and ascorbate peroxidase were overrepresented in dead glumes of wild emmer wheat. Thus our study highlighted previously unknown features of the dispersal unit in wild wheat in which the dead, hardened floral bracts enclosing the caryopsis store active hydrolases and nutritional elements and probably growth promoting substances that facilitate seed longevity and germination and increase seedling vigor.