Dormancy and germination of seeds are determined by various factors such as vitality, genotype, hardness, and other environmental cues, such as moisture, air, temperature, and light. Metabolic activity of seeds varies between the quiescent and imbibition state. In the dry state, longevity of a seed is determined by the reactive oxygen species (ROS) such as lipid peroxyl radical (LOO•) and lipid hydroperoxide (LOOH) that are generated nonenzymatically due to lipid peroxidation (LPO). During rehydration phase, enormous amount of ROS, such as superoxide (O2−), hydrogen peroxide (H2O2) and hydroxyl (•OH) radicals, are generated from the metabolically active compartments such as mitochondria, chloroplasts, and peroxisomes. The progressive conditional, temporal, and spatial distribution of ROS is tightly controlled by the effective antioxidant system that leads to the successful germination of seeds and this phenomenon is defined as ‘oxidation window.’ Gibberellins (GAs) and abscisic acid (ABA) are the key phytohormones involved in the germination/dormancy. Former promotes germination, whereas the latter induces dormancy. Genes involved in the synthesis and signaling of GA, such as gibberellin 3-β-dioxygenase (GA3ox), GA20ox, and GA-insensitive dwarf (GID), are responsible for the conversion of GA from an inactive to a bioactive form. On the other hand, DELLA, an important protein family acting as the repressors for GA-regulating genes, is activated by ABA. Function of genes, such as SLEEPY, PICKLE, SPINDLY, SECRET AGENT, AMYLASE, GAMYB, and LEAFY, are interrelated with the GA/ABA metabolism. By inducing the ubiquitin-26S proteolysis pathway, GA overcomes the DELLA-mediated effects on germination. The E3 ubiquitin ligase SCFSLY1 (skp1-cullin-F-box-Rbx1SLY1) complex was reported to be involved in the degradation of DELLA proteins. Additionally, cell differentiation and elongation process sustained by the ROS were also linked with the ethylene, brassinosteroids, and auxins. Hence, this chapter provides the heuristic framework on the phenomenon of systemic cross-talk between the ROS and phytohormones during the transition period of quiescent seeds into the metabolically active organisms.
- oxygen radicals
After pollination (double fertilization), the typical diploid embryos are covered by the triploid endosperm and the diploid testa. The triploid endosperm consists of nutritive tissues and living cells, while the diploid testa includes seed coat, maternal tissue, and dead cells. Seeds are the vital component allowing embryo dispersion and its consequent development into mature plants . The seeds of monocots and dicots differ in their structure and method of emergence [1, 2]. However, here we comprehensively focus on the signaling pattern of the reactive oxygen species (ROS) and its interaction during the germination and dormancy condition.
Although the dispersal of seeds is absolutely dependent on various cues such as vitality, genotype, hardness, moisture, air, temperature, light, and duration of seed storage, endosperm weakening is one of the key factors that determine the protrusion of radicle. The term “coat-associated dormancy” refers to the mechanical constraint that can impair germination, while “embryo dormancy” is characterized by the embryo failure to develop [1–3].
After imbibition, the weakening of endosperm is dependent on the gas exchange/respiration. Loosening of the endosperm was suggested to be influenced by the proper localization of ROS and its fine regulation by the antioxidant systems [4, 5]. The proper reduction/oxidation of the ROS (redox homeostasis) plays a key role in the transition from quiescence to active state . Gibberellins (GAs) are involved in the promotion of the endosperm weakening and, on the other hand, abscisic acid (ABA) at least partly inhibits this process either directly or indirectly [2, 3, 7]. Induction/inhibition of the genes responsible for the endosperm weakening is controlled by the ROS-GA-ABA [7–11]. Substantially, cross-talk of other phytohormones, such as ethylene, brassinosteroids and auxins, with GA and ABA were reported to be inevitable for the seed development .
Although research in seed biology has reached significant advancements, apparent continuum still lies in the mechanisms underlying germination and dormancy, which needs to be disclosed. In this chapter, the heuristic network on cross-talk between the ROS and phytohormones involved in the release and/or induction of dormancy has been discussed.
2. Seed Respiration
To fulfill the higher energy requirement during the transition period (from quiescent to active state) of the seed, cellular respiration is rapid, high, and synchronized with the mitochondrial activity . According to Law et al., proteins required for the biogenesis of mitochondria were already present in the dried seeds and this process is activated upon imbibition. Although the import of mitochondrial proteins is highly required for the biogenesis, amount of ATP consumption by mitochondria is limited as compared with other processes. On the other hand, amount of ATP required by the mitochondria for the protein import is lesser than the energy required for protein synthesis . In the transition period, oxygen (O2) released by the respiration governs the internal communications between the cell organelles and the rapid cell division and expansion . The excessive generation of ROS is extremely harmful to the cells. Although the O2− has very limited half-life (2 μs), the reduction in O2− (superoxide dismutation) results in the production of hydrogen peroxide (H2O2). Hydrogen peroxide can travel long distance and reaches the target as its half-life was determined to be about 1 ms. Other free radicals formed during the enzymatic reduction of O2− and H2O2 is •OH . The formation of •OH radical is mediated by iron in the Haber-Weiss and Fenton reactions. The uncoupled electrons present in the ROS cross-react with other essential metabolites or cellular components, affecting the normal cell physiology. However, a proper antioxidant system detoxifies the excessively generated free radicals and leads to the nondormant phenotype . Detailed mechanisms on the involvement of ROS in seed germination are discussed below.
3. Oxidation Window
During the embryogenesis and the seed-filling process, seeds possessed maximum water content . Subsequently, dramatic water loss takes place in the postmaturation stage . According to the recent reports, ROS do not play a detrimental role during development under controlled conditions . The ROS-mediated signaling is majorly involved in the endosperm weakening, mobilization of seed reserves, programmed cell death (PCD), and also protection against the pathogens . Hence, it can be ascertained that the ROS cannot be simply considered as a hazardous material. Controlled production of ROS and ROS-related molecular interactions represent key factors in various central components of plant biology . In the nondormant seeds, O2− and H2O2 radicals were uniformly distributed within the radicle, while in dormant seeds irregular patterns were observed. Only seeds with a proper redox homeostasis display nondormant phenotype [7, 11]. Success of the seed germination is apparently associated with the equilibrium between the ROS and its scavenging antioxidant system [1, 4–6]. Uncontrolled generation of ROS is extremely harmful and can lead to several lethal effects. Meanwhile, the tight control over the ROS helps in various developmental processes including germination. This process is generally termed as ‘oxidation window’ .
3.1. Quiescent seed
Quiescent seeds, characterized by low moisture content (5–15%), do not possess active metabolism. During the late embryogenic state, seeds are actively involved in the storage of reserves, while enzymatic activities are gradually decreased. However, during the storage, lipid peroxidation (LPO) occurring on the polyunsaturated fatty acids (PUFA) in the cell membrane constantly releases the ROS [2, 3]. Longevity of seeds depends on the free radicals generated by the LPO. In the dried condition, ROS are released from polyunsaturated fatty acids by LPO . The free radicals focused on the H-atom in the methyl group of lipids. The single cleavage leads to the release of LOO•, and the double cleavage leads to the release of LOOH . Depending on the aging extremity, ROS affects the viability of the seed. Most of the enzymatic activities are arrested in the dried state of the seed. Damages caused by LPO cannot be retained during the transition from a quiescent to an active state [19, 20]. From the epigenetic study of Nakabayashi et al., it can be suggested that more than 12,000 stored mRNA species or transcripts were detected in the desiccated seeds of
3.2. Imbibed seed
In general, germination normally begins with the imbibition of seeds by 70–80% of water. El-Maarouf-Bouteau and Bailly reported that high levels of ROS are accumulated during the imbibition phase . This might be due to the resumption of metabolically active sites such as mitochondria, chloroplasts, peroxisomes, glyoxysomes, and plasma membranes. The mitochondrial electron transfer chain (ETC) was considered as a primary source for the ROS (O2−). Foyer et al. reported that 2–3% of oxygen from the mitochondria was the source of O2− and H2O2. In addition, chloroplast, a vital site for photosynthesis, and ETCs from the photosystems, such as PSI and PSII, produce O2
The hydrated state of seeds allows the longer shelf life H2O2 to reach the targets distant from the production sites . As mentioned earlier during the unfavorable condition, ROS lead to the breakdown of essential macromolecules such as lipids, nucleic acids, proteins, and other deleterious activities . In the favorable condition, the ROS stimulates the mobilization of reserves and selectively interact with the targets by oxidation. This oxidation triggers a gene-specific signaling pathways and also activates the transcription factors (TFs) either directly or indirectly [15, 19, 20]. The cleavage of cell wall-polymers of endosperm can be correlated with the over-expression of cell wall-peroxidases . During the putative shift from the desiccation to the germination state, exogenous application of optimal H2O2 increased the regulation of 113 genes and decreased the regulation of 62 genes in
3.3. Temporal and spatial regulation of ROS accumulation
The metabolically active sites are the source of ROS. As the range and action of ROS are limited by diffusion, ROS production source determines its molecular mobility and viscosity . The rate of metabolic activity and the source of ROS production govern the process of seed development. Leymarie et al. reported that after imbibition, the ROS are first localized in the cytoplasm followed by the nucleus and lastly in the cell wall . In the cytoplasm, ROS modulates the redox homeostasis which triggers the protein oxidation and mRNA synthesis is the first sign of seed germination process [30–32]. Antioxidant systems are concordantly involved in maintaining the ROS level. The fine tuning of the ROS is achieved by the direct or indirect interaction with the transcription factors of the genes responsible for the redox status. Finally, the NADPH oxidase located in the cell wall helps in cell-to-cell propagation . In the dormant phenotype, ROS production is high and also scattered. In the dormant phenotype, the ROS is properly diffused from cytoplasm to nucleus and cell wall . The role of ROS (either beneficial or deleterious) is dependent on its distribution. Therefore, the temporal and spatial accumulations of the ROS are inevitable for proper germination [15, 29].
3.4. Protein carbonylation
Seed vigor is mainly affected by the protein oxidation process such as carbonylation and decarbonylation. Protein carbonylation is the oxidation of proteins caused by the ROS, especially on the side chains of lysine, arginine, proline, and threonine . Decrease in the carbonylation of proteins is known as decarbonylation . Activation on the oxidation phase of pentose phosphate pathway (oxPPP) modulates the carbonylation of proteins. Modulation of redox potential in the glycolysis and oxPPP were observed during the release of dormancy . The interaction or signaling of the ROS determines or fine tunes various translation and posttranslation processes during the seed development. Job et al. reported that in the dry seed, proteins, such as 12S-cruciferin subunits, aldose reductase and the LEA, undergo carbonylation. After imbibition, protein carbonylation specifically targets glycolytic enzymes, mitochondrial ATP synthase, chloroplastic ribulose carboxylase large chain, aldose reductase, methionine synthase, translation factors, and molecular chaperones . The NADPH-oxidase also known as respiration burst oxidase homolog (rboh) plays an important role in the transfer of electrons from cytosolic NADPH or NADH to apoplastic oxygen and posttranslational modifications of proteins. In Arabidopsis,
3.5. Antioxidant enzymes
As mentioned earlier, improper desiccation as well as storage increases the LPO and affects seed vigor. Increased production of ROS from the metabolically active sites during the transition from a quiescent to imbibition state could possibly cause stress. The deleterious effects of the ROS can be overcome by the proper antioxidant system. Both enzymatic and nonenzymatic antioxidants play a vital role in the maintenance of level of the ROS. Rather than complete alleviation, proper activation of antioxidant enzymes directs the ROS to the signaling process [24–27]. Muller et al. reported that ROS are important components in the endosperm weakening . Exogenous application of H2O2 or menadione (to generate superoxide) to 3-day old maize seedlings enhances tolerance against the chilling stress . Meanwhile, Pulido et al. found that nuclear localization of peroxiredoxin and thioredoxin prevents nucleic acids from oxidative damage occurring during the maturation and germination in wheat seeds . The detoxification of H2O2 in the seed filling is catalyzed by the isoforms of catalase (CAT). The isoform CAT3 is involved highly in the early postpollination, whereas CAT1 and CAT2 isoforms play a crucial role during the seed development [41, 42]. Recently, Leymarie et al. clearly demonstrated the necessity of the ROS and the antioxidant enzymes for successful germination using mutant seeds. In the
3.6. Nonenzymatic antioxidants
Nonenzymatic antioxidants that actively participate in the ROS equilibrium are ascorbate, glutathione, and preoxiredoxins [44–47]. Low moisture content decreases the molecular mobility and the accessibility of substrates for the catalysis of antioxidant enzymes . Ascorbate plays a major role in the progression of cell cycle, cell growth, hormonal signaling pathways, and embryogenesis. Ascorbate content of the seed decreased the H2O2 by increasing the peroxiredoxins . Nonenzymatic antioxidants also determine the protection of cells against the ROS, particularly at the desiccation stage. Tocopherol is involved in the prevention of membrane damages by the LPO during a prolonged seed storage . Peroxiredoxins protect the nuclear integrity and prevent against the oxidative damages of DNA under high levels of •OH radicals . Involvement of the ascorbate-glutathione cycle alone in the seeds could be another vast area, which needs to be discussed separately.
3.7. Interplay between ROS, GA, and ABA
It has been proven that an inhibitor of the ROS, sodium benzoate, decreases the germination rate of the seed . Diphenylene iodonium (DPI), an inhibitor of NADPH oxidase, also affects the germination rate . On the other hand, methylviologen, involved in the release of superoxide from the mitochondrial respiratory chain breaks the seed dormancy . Capacity of seeds to germinate or remain dormant is determined by the two important phytohormones such as GA (dormancy release) and/or ABA (dormancy induction). Bailly et al. reported that GA and ABA are interlinked with the ROS and the scavenging capacity of antioxidant enzymes . Generally, GA is mainly used for the dormancy release, while ABA induces the dormancy. The GA is involved in the stimulation of •OH production, especially in the radicle, and it also downregulates the enzymes involved in the ROS detoxification. Contrastingly, ABA inhibits the Fenton reaction, where the iron (II) is oxidized by the H2O2 to form the iron (III) and the release of •OH . The processes of seed germination and dormancy are linked with ROS accumulation . The productions of H2O2 in the sunflower are higher in the germinating seeds than the dormant seeds . Similar results have been observed by comparing the dormant and nondormant seeds of many plants, such as
3.8. Protection against pathogens
The release of the ROS in the seeds during the development period protects the seeds against pathogens. It also induces the systemic-acquired resistance (SAR) and PCD. Especially when the ROS is mobile toward the seed coats, aleurone layers, and embryonic axis, the attack of microorganism is prevented by the induction of SAR and PCD [19, 61]. Briefly, the plasma membrane NADPH oxidase produces O2−, which is converted into H2O2 by SOD during the infection. Subsequently, H2O2 induces a hypersensitive reaction which leads to PCD of the infected cell. Eventually, H2O2 can also directly affect the pathogens [62, 63]. The main categories of genes involved in the H2O2 induction are related to defense, transcription, signaling (e.g., phosphatases, kinases), and importantly ROS synthesis and degradation. Perturbation of endosperm for the radicle emergence leads to the induction of defense-related genes. It helps to protect the newly germinating seeds from the pathogens . During the seed germination process, lower concentrations of the ROS are involved in the cell signaling process, whereas higher concentrations trigger the PCD to facilitate the radical protrusion .
3.9. Endosperm weakening
Proteolytic cleavage of cell wall polymers is induced by the hydrolases such as mannose, glucanase, and cellulose. The scission of polysaccharides is a vital step to determine the radicle emergence. According to Muller et al., •OH accumulation is the main factor, which influences endosperm weakening by the breakdown of H-bonds in the cell wall-polysaccharide required for the radicle protrusion. Generally, •OH is extremely reactive and is considered as the most aggressive form of oxygenated derivatives . Uncontrolled ROS accumulation affects the integrity of DNA, causing changes at the sequence level that impair proper seed germination and could be able to change the genetic code of the seeds. The O2− and H2O2 seem to be less reactive toward nucleic acid as compared to •OH . However, cellular dysfunctions caused by ROS accumulation can be prevented by the antioxidants .
Oxidative damages caused by excess ROS are irreversible. The progressive conditional, temporal, and spatial distribution of the ROS tightly controlled by the antioxidant system leading to seed germination are also defined as ‘oxidation window’ (Figure 1).
4. Molecular Network of Gibberellins and Abscisic Acid in Germination/Dormancy
As mentioned earlier, germination and dormancy release of seeds are governed by the GAs and ABA. According to previous reports, although there are many factors involved in seed germination, GA and ABA biosyntheses have been considered as an important internal factor for the release as well as the induction of dormancy . Metabolisms of ABA and GA is always interrelated . Seo et al. reported that
4.1. Dormancy breakage
Gibberellins are majorly responsible for the breakdown of dormancy . However, in the later phase of embryogenesis, i.e., during the maturation drying, GA production must be reduced and ABA synthesis is upregulated for the proper maturation and to preserve seed vigor. During the imbibition stage, the endogenous GA1 is released from the viable nondormant embryo to its endosperm. It increases the activities of several enzymes, such as amylase, proteases, ribonucleases, and β-glucanase, which induce the hydrolytic cleavage in the aleurone layer . Moreover, hydrolytic enzymes are also involved in the transcription, transportation of metabolites, and PCD. Along with the GA biosynthesis, genes encoding for various functions are either overlapped or attributed toward the germination, and this process is controlled by the GA [66, 67]. Moreover, genes encoding gibberellin 3-oxidase (
Higher expressions of cell wall-remodeling enzymes (CWRE) is associated with the radicle protrusion. Endo-β-mannanase, β-1,3-glucanase, expansin, xyloglucan endo-transglycosylase, pectin methylesterase, polygalacturonase, and galactanase are the notable major enzymes involved in the cell-wall modification . In
4.2. Dormancy induction
Enhanced dormancy occurred when the ABA content was increased in the
The ABA was involved in the vacuolation process to inhibit the endosperm loosening rather than the lipid breakdown . Recently, it was found that the loss of function of the gene coding for E3 ligase ABI3-interacting protein 2 (AIP2) and ABI3-binding factor protein (AFP) leads to the ABA insensitivity and the nondormant phenotype even in the presence of ABA. Major receptors of the ABA are pyrabactin resistance1 (PYR1), PYR1-like protein (PYL), and regulatory components of ABA receptors (RCAR). Those loci encoding the main players in the ABA metabolism are also associated with the RNA translation and metabolism, protein-degradation pathways, and phosphatase components of the signaling pathways [69–75].
4.3. DELLA proteins
The DELLA proteins [GA insensitive (GAI), repressor of ga1-3 (RGA), and RGA-like proteins (RGL 1-3)] belong to the subfamily of plant-specific Glycyl-TRNA synthetase (GRAS) proteins. The name of GRAS proteins was derived from the initially identified members such as
Recent research found that the GA signal inactivated the functional domain of DELLA protein. The GA induced repression of the RGA through protein degradation rather than the blocking of translational process . The deletion of the conserved motif VHYNP present in the DELLA region or the region between the VHYNP-DELLA, releases the dormancy by enhancing GA metabolism. Additionally, GA-dependent degradation of proteins is also associated with
DWARF, SLEEPY, PICKLE, SPY, and SECRET AGENT
The presence of GA at higher levels makes the plant thin and watery. Contrastingly, lack of GA-biosynthetic genes or lesser amount of endogenous GA produces the thicker leaves with dwarf shoots. It was previously reported that GA-unresponsive dwarf phenotypes were observed in mutants such as
AMYLASE, GAMYB, and LEAFY
The enzyme amylase plays an important role in the hydrolysis of endosperm starch into usable sugars. This provides the necessary energy for the emergence of radicle. Plants possess both alpha (α)- and beta (β)-amylases. The expression of α-amylase in the aleurone layer is induced by GA. Activation of the
5. Role of Other Phytohormones in Seed Germination/Dormancy
Ethylene was reported to be involved in various metabolisms such as dormancy breakage, root induction, defense against pathogens, and signaling . Precisely, 1-aminocyclopropane-1-carboxylate oxidase (ACC oxidase), a precursor of ethylene synthesis, is required for higher synthesis of H2O2. Mutant lacking the GA synthesis gene (
Brassinosteroids are well known for their functions in the cell elongation, cell cycle, and various other metabolisms. They are involved in the enhanced expression of
Auxins are generally known for their roles in the root induction. Ogawa et al. reported upregulation of a number of auxin biosynthetic genes and genes encoding for auxin-carrying proteins in response to exogenous GA4 application . The GA was well known to promote the auxin synthesis and the transportation of ethylene. Chiwocha et al. (2005) evidenced that the interaction of ethylene biosynthetic genes with the auxin signaling genes such as
During the developmental stage of embryos into the vigorous photoautrotropic organisms, numerous metabolic processes are activated and they include oxidation of proteins, cellular structural changes, and synthesis of macromolecules. The cascade of metabolic process ceases with the development of the radicle governed by the well-directed ROS accumulation. Interlinked relation between the GA and ABA aids in the proper development of the embryo, seed filling, desiccation tolerance, imbibition, hydrolysis, temporal and spatial distribution of ROS, proteolysis, and radicle protrusion. The recent evidences suggest that ABA-GA cross-talk with other phytohormones, such as ethylene, brassinosteroids and auxin, could play a vital role in the development of the seed. The important components other than the free radicals such as O2-, H2O2, and •OH pertaining to the seed potential is the NO. Tapping of the NO linked with the GA-ABA and their responses to the light and temperature could be one of the interesting areas getting more attention on the seed research.
Prabhakaran Soundararajan and Abinaya Manivannan were supported by a scholarship from the BK21 Plus Program, the Ministry of Education, Republic of Korea.
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