Cereal Husks: Versatile Roles in Grain Quality and Seedling Performance

Abstract

The seed is the fundamental unit of the dispersal of dry, dehiscent fruits, in which the fruit splits open at maturity to allow for seed dispersal. However, dry fruits may be indehiscent and therefore represent the dispersal unit (DU). Cereals possess a one-seeded fruit, whereby the seed coat and the fruit coat are fused together to generate the caryopsis. This caryopsis may be covered by floral bracts to generate two types of DUs, namely florets, whereby the caryopsis is enclosed by the lemma and the palea (e.g., Avenasterilis) or spikelet, whereby the floret(s) is further covered by the glumes (Triticum turgidum var. dicoccoides). Here, we highlight the dead coverings enclosing the caryopsis in cereals, namely the husks as an integral component of the dispersal unit that play multifaceted roles in grain biology. Thus, besides protection and dispersal means, the husks function as a rich maternal supply of proteins and metabolites for enhancing growth and development, combat potential pathogens as well as confer tolerance to abiotic stresses. These attributes might have broad implications for crop performance, plant population dynamics and diversity in ecological systems, and for conservation of genetic resources in seed banks.

1. Introduction: Dispersal Units of Cereals

Seed quality is the sum of all characteristics that contribute to seed fate and performance. It is commonly determined by several parameters including genetic, physical and physiological qualities and storability [1]. The seed is the basic unit of dispersal in plants, and it is at the focal point of farmers, seed companies, seed banks and the food industry. In addition to the seed that represents the dispersal unit (DU) of dry dehiscent fruits, a variety of DUs have evolved in plants including dry indehiscent fruits, whereby the fruit does not split open at maturity and often represents the dispersal unit from which seeds are germinated [2,3]. Cereals have evolved unique and variable DUs in which the fundamental unit is the caryopsis, a fruit containing a single seed, which can be further enclosed by the dead floral bracts, lemma, palea and glumes. Thus, the DU in cereals can be composed of the fruit (caryopsis) only (e.g., Sporobolus species, commonly called ‘dropseeds’), florets in which caryopses are enclosed by lemma and palea (e.g., Avena species), spikelets where the florets are further enclosed by the glumes (e.g., Triticum turgidum var. dicoccoides; Hordeum spontaneum) and the whole spike may serve as a DU (Aegilops species). Notably, in certain species (e.g., Tripsacum dactyloides), the DU is composed of the spikelet and its adjacent invaginated internode that generate a cupule-like structure enclosing the caryopsis [4]. Wild Poaceae species are readily germinating from the whole DU and the husks do not necessarily pose a physical barrier for germination (Figure 1). The DUs of cereals are often equipped with hygroscopic awns that contribute to DU orientation during its fall from the mother plant, movement across the soil surface and positioning of the DU in the soil [5,6,7,8]. While the term dispersal unit highlights its major role in seed dispersal, it carries multiple functions including embryo protection, moisture adsorption, light filtering, regulation of seed respiration and seed dormancy [9].

2. The Role of Husk and Other Dead Coverings in Seed Biology and Ecology

Multiple reports have addressed the effect of dead floral bracts (husks) of Poaceae species on seed germination, showing that it is variable and species/cultivar dependent. Thus, the husk could have a negative effect on germination inasmuch as the removal of husks improved the seed germination of various grasses including Aegilops species [10,11], the saw-grass Cladium jamaicense [12], Indica rice (Oryza sativa L.) cultivar [13], Leymus chinensis [14], Zoysia japonica [15] and of buffalo grass [16]. Similarly, improved germination has been reported for Zinnia elegans (Asteraceae) [17] and the crucifers Lachnoloma lehmannii [18] and Sinapis alba [3] upon removal of the pericarp. Most common explanations for the negative effect of husks on germination include the exertion of seed dormancy or mechanical barriers that limit oxygen and water uptake as well as embryo growth during germination [4,19,20]. Conversely, multiple reports highlighted the positive effect of dead organs enclosing the embryo (DOEE) on seed germination and seedling performance. Accordingly, the seedling establishment of Eurotia lanata (Amaranthaceae) was significantly higher when germinated from intact fruits than from trashed seeds [21] and the pericarp of Hedysarum scoparium L. (Fabaceae) was shown to contribute to seed longevity and seedling establishment in arid environments [22]. Similarly, various Poaceae species displayed better germination and/or seedling establishment when germinated from the intact DU. The husk of Avena sterilis (winter wild oat) and Triticum turgidum var. dicoccoides (wild emmer wheat) profoundly improved seed germination performance and fate, showing faster and more homogenous germination/emergence from the whole DU compared to naked caryopses as well as enhancement of seedling vigor [23,24]. The germination of Japonica rice was higher for intact seeds (caryopsis enclosed by the husk) than de-husked seeds [25], while seedlings of Brachypodium hybridum emerged from husked grains display better growth than seedlings of de-husked grains [26].

It is worth noting that DOEEs/husks have a broad effect on seed quality, affecting not only germination but also post-germination growth and development. Thus, reported data addressing the effect of DOEEs/husks on germination per se should not be immediately interpreted into a positive or a negative plant attribute or into agricultural/environmental practices without addressing the fate of germinating seeds and seedling performance. Accordingly, the finding that husk removal improved the seed germination of Microlaena stipoides and Rytidosperma geniculatum to some extent should not be turned into a practical procedure that ‘will facilitate more efficient grassland restoration at large scale’ [27] before addressing the post-germination effects and seedling performance. Indeed, germination assays of naked caryopsis of wild emmer wheat was accelerated compared to germination from the whole DU, yet seedlings from the whole DU performed significantly better than naked caryopsis seedlings [23]. Moreover, while the final germination of husked and de-husked grains of Brachypodium hybridum was similar, husked grain seedlings grew better than de-husked seedlings [26].

Homogenous germination and improvement of post-germination growth conferred by the husk might have implications for successful seedling establishment and high vigor in agroecosystems. The significance of husks in seed quality is highlighted in barley grains, which are commonly used for malt preparation. The barley grain is composed of a caryopsis which is strongly adhered to the husk, the lemma and the palea, which characterize the grain germination capacity and malting quality. Upon harvesting, the husk is often damaged or detached, leading to the undesired phenomenon known as ‘grain skinning’. This phenomenon significantly reduces grain quality, resulting in increased damage to the embryo and irregular germination with a significant negative economic impact on the malting industry [28,29].

3. Husks Function as Long-Term Storage for Beneficial Substances

How do dead husks improve the performance of seeds and seedlings? At maturation, all maternally derived organs enclosing the plant embryo including seed coat, pericarp and floral bracts in cereals undergo programmed cell death (PCD) [30,31,32], a physiological process that controls the degradation of almost all macromolecules such as DNA, RNA and proteins and whose constituents are remobilized mostly to filial organs [33,34,35]. Yet, recent reports have demonstrated that organs enclosing the embryo undergo a highly regulated PCD whereby hundreds of proteins remain intact and persist in an active form for decades and are released upon hydration to the immediate surrounding of the dispersal unit [36,37].

Detailed analysis of husks was performed for A. sterilis and wild emmer wheat. Proteome analysis of a dead husk of A. sterilis and dead glumes of wild emmer wheat uncovered hundreds of proteins, many of which are involved in metabolic processes and in oxidation–reduction processes as well as in response to stress [23,24]. Some enzymes, such as cell wall-modifying enzymes and ROS-detoxifying enzymes, found in husks may contribute to seed germination and seedling establishment [38,39,40,41], while nucleases, chitinases and proteases [24] may act against potential soil pathogens [42,43,44,45]. Interestingly, the composition and level of multiple proteins accumulated in Avena husks were significantly changed under drought conditions. Many proteins related to the response to stress were significantly up-accumulated in husks derived from mother plants grown under water deficit [26], including the chitin-binding type 1 protein involved in the ethylene/jasmonic acid signaling pathway during systemic acquired resistance [46], the thioredoxin domain-containing protein, induced in response to oxidative stress [47], as well as members of the small heat shock protein (HSP) group that play an importance role in tolerance to multiple types of stresses [48,49]. Thus, proteins accumulated in husks may facilitate germination and provide a primary defense layer against anticipated biotic and abiotic stresses, and consequently improve seed quality.

Husks of A. sterilis plants as well as glumes of wild emmer wheat possess multiple phytohormones such as jasmonic acid (JA), salicylic acid (SA) and abscisic acid (ABA) [24], known to participate in plant stress response and immunity [50,51,52,53]. In addition, the glumes of L. chinensis accumulate various phytohormones including GA3, ABA, IAA, and zeatin [54]. ABA was particularly up-accumulated in Avena husks derived from mother plants subjected to drought conditions [24], probably reflecting the physiological state of Avena plants in response to water deficits [55]. SA, JA and ABA might be released upon hydration and prime the germinating seeds for both biotic and abiotic stresses [52,53,56].

The husks also accumulate allelopathic or promotive substances that selectively inhibit or promote seed germination, respectively. Considering the accumulation of phytohormones in husks, it is possible that part of the effect on seed germination is controlled by ABA and GA, which act antagonistically to inhibit or promote germination, respectively [57]. Fresh extracts of the glumes of Aegilops kotschyi and hulls of Avena fatua inhibited the germination of lettuce seeds [58,59]. Indeed, the glumes and hulls of Aegilops kotschyi possess a coumarin- or abscisin-like germination inhibitor that affects gibberellin (GA) metabolism [10]. The glume extract of L. chinensis significantly inhibited the germination and root length of Chinese cabbage, showing no effect on the seed germination of L. chinensis [54], and the husks of A. sterilis possess substances that specifically inhibit the seed germination of Sinapis alba but not of Brassica juncea [24]. Furthermore, crop residues of Sorghum cultivars including glumes contain allelopathic substances that inhibit wheat seedling growth [60]. Selective allelopathy [61,62] provides a means for reducing competition for resources [63] on the one hand and permits seed germination of other species for facilitative plant–plant interaction on the other hand [64]. Seed germination of Codonopsis pilosuala was dramatically enhanced under rice hull cover treatment [65] and rice hull was found to induce dark seed germination of Monochoria vaginalis, a noxious weed commonly requiring light for germination [66]. Interestingly, only unsterilized Monochoria seeds were able to germinate in the darkness by rice hull extract, leading to the conclusion that rice hulls might promote microbial growth that acts to weaken the seed coat and consequently facilitates germination [66]. Indeed, DOEEs were found to accumulate substances that affect microbial growth in a species-dependent manner. Avena husks as well as S. alba and B. juncea pericarps contain substances that significantly enhance bacterial growth [3,24,67], while pericarps of the desert crucifer Anastatica hierochuntica contain substances that strongly inhibit microbial growth [68,69]. The differential effect of DOEEs on microbial growth may be related to the mode of interaction between plants and their distinct habitats, as well as the co-evolution with their specific microbiota. Microbes whose growth is stimulated by substances released from the husk could in turn provide plants with growth regulators and defense inducers [70] that assist survival and plant growth and development.

It should be mentioned, however, that husk biochemical properties have changed in the course of domestication, and variation between wild plants and domesticated cultivars was reported [23].

4. The Husk and Storability of Seeds in Seed Banks

The storability of the genetic material of various crop cultivars and wild relatives (e.g., cereals) is of prime importance, with the main goal of preservation of the evolutionary constituents of a given species or genus in term of allele and gene diversity for future usages [71]. There are two major strategies for genetic resource conservation, namely in situ, that is the conservation of species in their natural surroundings, and ex situ, the conservation of species outside of their natural ecosystem, particularly in seed banks [72]. Seed conservation in seed banks requires an appropriate facility for long-term preservation under dry, cold conditions, to ensure the reduction in metabolic activities and consequently an increase in seed longevity over periods of years and even decades [73]. Notably, ageing processes are not completely blocked under seed bank conditions and seeds may lose their quality and viability [74]. Seed bank protocols demand a cleaning stage whereby seeds or caryopses are commonly separated from their natural coverings (pericarps, or lemmas, paleas and glumes in cereals) that constitute the dispersal unit for sanitation purposes and for saving storage space [75]. Considering the importance of DOEE/husk for seed fate and seedling performance, these cleaning steps employed by seed banks should be revisited. To date, no detailed study has been conducted to explore the significance of dead coverings (husk, hull, pericarp) in seed longevity and viability under conservation conditions in seed banks. In a recent review on seed quality in seed banks, Rao et al. [76] described various agronomic approaches with the potential to improve seed quality and the longevity of stored seeds in seed banks. In this review, few examples from past studies are given, which imply the possible role of seed coverings (glumes, shells etc.) in maintaining seed quality. Multiple factors may influence the lifespan of seeds, including genetics, preharvest growth conditions, seed maturity, storage conditions and seed structure and composition [77]. Early work on factors influencing the lifespan of grass grains highlighted the importance of dead floral bracts (glumes, lemmas and paleae). Accordingly, the viability of aged seeds of barley cultivars and red winter Speltz wheat with hulls was higher than trashed seeds of the same harvest [78]. Similarly, timothy (Phleum pratense L.) seeds with hulls performed better and had a longer lifespan than naked seeds [79,80].

5. Conclusions

Seeds, in general, are the most desired product of plant sexual reproduction and are at the focal point of farmers, seed companies, seed banks and the food industry. Seeds represent the fundamental unit of dispersal in higher plants, yet a large variety of dispersal units have been developed where the seed is further enclosed by maternally derived dead organs, such as pericarps (indehiscent fruit) or floral bracts (lemma, palea, glume) in cereals. DOEEs have long been viewed as a physical shield for embryo protection capable of regulating seed germination and seed dispersal. In recent years, the importance of the DOEEs/husk in seed biology and ecology has been gaining attention as they appear to serve as a storage unit of maternal supply destined for progeny seeds, including proteins that can retain enzymatic activities and other substances, such as phytohormones, sugars and amino acids, to ensure offspring success and survival in the habitat. Obviously, the dead husks of cereals which were evolved in each species in conjunction with its unique habitat represents a functional component of the dispersal unit, which determines the overall quality of the seed. Thus, in addition to the genetic makeup of the embryo, which represents a major component contributing to seed fate and performance, the maternally derived husks and the supply of substances embedded within the husks, in the form of proteins and metabolites, add other non-genetic features that together contribute to embryo protection, seed dispersal as well as to longevity and storability (seed banks) and consequently to seed viability and seedling vigor (Figure 2). This might have implications for various ecological and agricultural practices, including the restoration of disturbed grasslands, organic agriculture (husk as a natural coating that increase vigor) and ex situ conservation of genetic resources in seed banks. A detailed study should be conducted to address the costs and benefits of conservation in seed banks of the whole dispersal unit over naked seeds and the consequences for seed longevity, germination and seedling establishment. Finally, husks are major crop residues produced in gigantic quantities worldwide, making their valorization a topical issue in recent years. The beneficial properties of husks as rich sources for minerals, growth factors, antioxidants, proteins and other beneficial substances should further stimulate its utilization as a by-product for various purposes, including soil amendment, animal feed, production of biochar, as well as a resource for valuable substances [81,82].