Abstract

Reactive oxygen species (ROS) are versatile compounds which can have toxic or signalling effects in a wide range living organisms, including seeds. They have been reported to play a pivotal role in the regulation of seed germination and dormancy but their mechanisms of action are still far from being fully understood. In this review, we sum-up the major findings that have been carried out this last decade in this field of research and which altogether shed a new light on the signalling roles of ROS in seed physiology. ROS participate in dormancy release during seed dry storage through the direct oxidation of a subset of biomolecules. During seed imbibition, the controlled generation of ROS is involved in the perception and transduction of environmental conditions that control germination. When these conditions are permissive for germination, ROS levels are maintained at a level which triggers cellular events associated with germination, such as hormone signalling. Here we propose that the spatiotemporal regulation of ROS production acts in concert with hormone signalling to regulate the cellular events involved in cell expansion associated with germination.

Introduction

Oxygen supports aerobic life, but can also give rise to the reactive oxygen species (ROS). These include free radicals, such as singlet oxygen (1O2), superoxide (O.−2) or hydroxyl radical (·OH), and hydrogen peroxide (H2O2), which is not a free radical. Hydrogen peroxide is considered as the main ROS involved in cellular signalling as it is rather stable (lifetime of milliseconds) in cellular conditions and is capable of crossing biological membranes [1]. Although ROS have distinct chemical properties, they are all highly reactive and can cause damage to other biomolecules. Oxidative stress is well documented in higher plants since it generally accompanies biotic and abiotic stresses and can ultimately lead to cell death [2]. In contrast, ROS are also recognized as key signalling intermediates involved in a wide range of plant responses to the environment and as regulators of plant development [3,4].

More than a decade ago it was proposed that ROS were involved in the control of seed germination and dormancy release [59]. At this time, ROS were principally known as being responsible of oxidative damage and loss of viability during seed ageing [10]. The involvement of ROS homeostasis in regulating seed germination came in 2007 when Oracz et al. [11] demonstrated that ROS triggered protein carbonylation to release dormancy. ROS thereafter progressively emerged as essential components of the germination process leading to the concept of ‘oxidative window for germination', which restricts the occurrence of the cellular events associated with germination to a critical range of ROS level, enclosed by lower and higher limits [9]. There is now further evidence showing that ROS homeostasis is critical for germination, and this is examined in this review article.

Seeds are spectacular and intriguing organisms. They are at the core of plant kingdom because they retain the genetic information of higher plant species, which survival and dissemination depend on seed longevity and successful germination. Seeds have some particularities which must be considered when investigating the role of ROS in their germination. First, the so-called ‘orthodox seeds' desiccate on the mother plant at the end of their developmental program, reaching very low moisture content [12]. This desiccation phase can be considered as an extreme drought stress associated with ROS generation and oxidative stress, from which developing seeds are protected through enzymatic and non-enzymatic mechanisms [7]. As a consequence, at shedding, the status of dry mature orthodox seeds is largely oxidized. The physiology of dry mature seeds then evolves during their subsequent dry storage. In particular, this dry storage period can alleviate dormancy, a blockage of germination in apparently favourable environmental conditions, in a process termed after-ripening [13]. Desiccated seeds are resting organisms where no metabolism can be detected, but non-enzymatic ROS generation has been frequently evidenced in these conditions [11,14,15]. Secondly, during seed imbibition, water uptake allows metabolism resumption and radicle protrusion, the first visible sign of germination, if the environmental conditions are permissive, i.e. if water potential, temperature, oxygen and light conditions are appropriate, and if seeds are non-dormant [13]. The recovery of an active metabolism is associated with enzymatic and regulated production of ROS. In contrast with the whole plants, imbibed seeds are very sensitive to small variations of environmental factors. This sensitivity is an adaptive trait which allows germination to proceed only in conditions appropriate for subsequent seedling development, thus increasing the probabilities of survival of the resulting seedlings. For example, a difference of few degrees Celsius can impose a block of seed germination, a phenomena which is emphasized in dormant seeds [16]. This suggests that environmental signals must be accurately transmitted to seeds and translated into endogenous signals regulating germination. In this review we propose that ROS are very good candidates for fine-tuning germination. Lastly, the relationship of ROS with other cell signalling pathways, i.e. plant hormones, is often different in seeds than in other plant systems. For example, abscisic acid (ABA) and ROS interact synergistically in response to plant abiotic stress such as drought, in particular for regulating stomata opening [17], but in seeds ROS and ABA are generally antagonists. This particularity has also to be considered when studying ROS signalling in seeds.

The objective of this review is to provide a critical view of the signalling role of ROS in seed germination and dormancy, taking into account the recent findings in both germination and ROS signalling mechanisms.

Evidence for a role of ROS in germination and dormancy

Table 1 [11,1863] displays some of the works dealing with the signalling role of ROS in seed germination and dormancy that have been published these last ten years. In this table, we have distinguished the beneficial and detrimental effects of ROS accumulation on the completion of germination or on dormancy release. It appears clearly that most of these works have evidenced a positive role of ROS in these processes, whatever the species, which suggests that controlled ROS accumulation during seed imbibition is a prerequisite for radicle elongation, as well as for dormancy alleviation, whatever the seed dormancy release treatment (cold stratification or after-ripening). In this context many attempts have been performed in order to investigate whether ROS homeostasis cross-talk with the major hormonal regulators of germination and dormancy, i.e. ABA, gibberellins (GA) or ethylene, and the major findings are discussed below. In contrast, some studies have also shown that ROS accumulation could also delay or an inhibit of seed germination, without causing cell death. Such effects have been evidenced when seeds were germinated in stressful conditions either caused by drought, salt stress or toxic compounds in the imbibition medium, for example (Table 1), i.e. when conditions of seedling development were not favourable. This demonstrates that the signalling role of ROS in seed germination is not always associated with a stimulation of this process.

Table 1
Reported effects of ROS on seed germination
ContextEffectSpeciesReference
Zn and Arsenic stress negative Anadenanthera peregrina and Myracrodruon urundeuva [18
Germination positive apple [19
Dormancy alleviation (stratification) positive apple [20
Salt stress negative Arabidopsis [21
ABA cross-talk ABA positive regulator of rboh and ROS Arabidopsis [22
Cd Stress negative Arabidopsis [23
Mitochondrial functionning positive Arabidopsis [24
Salt stress positive Arabidopsis [25
Seed dormancy and iron deficiency positive Arabidopsis [26
Germination/ABA negative Arabidopsis [27
Salt stress/ethylene negative Arabidopsis [28
Germination/light positive Arabidopsis [29
Dormancy positive Arabidopsis [30
Germination/ABA/AIA positive Arabidopsis [31
Germination ABA GA positive Arabidopsis [32
Germination/ABA signalling positive Arabidopsis [33
Dormancy ABA GA positive barley [34
Seed germination and dormancy positive barley [35
Germination/ABA signalling positive barley [36
Dormancy alleviation positive barley [37
Germination/GA/NADPH oxidase positive barley [38
Germination/NADPH oxidase positive barley [39
Dormancy positive Bidens pilosa [40
Dormancy alleviation (stratification) positive Bunium persicum [41
Dormancy alleviation (stratification) positive Hedysarum scoparium [42
Germination/endosperm weakening positive lettuce [43
Mutagen agents negative maize [44
Dormancy alleviation by heat positive Mesembryanthemum crystallinum [45
Drought and salt stress negative Miscanthus [46
Germination/ABA positive pea [47
Germination positive Pea [48
High temperature, drought stress negative rice [49
Low phytic acid seed vigour positive rice [50
Dormancy alleviation (after-ripening) positive rice [51
Germination/NADPH oxidase positive rice [52
Osmotic and salt stress negative rice [53
Germination/ABA/GA positive rice [54
Germination/ethylene positive soybean [55
Dormancy alleviation (after ripening) positive sunflower [56
Dormancy alleviation/ABA/ethylene positive sunflower [57
Dormancy/after-ripening positive sunflower [11
Dormancy positive sunflower [58
GA response positive tobacco [59
Germination positive Vigna radiata [60
Germination positive Vigna radiata [61
Seed vigour and GA signalling positive watermelon [62
Dormancy positive wheat [63
ContextEffectSpeciesReference
Zn and Arsenic stress negative Anadenanthera peregrina and Myracrodruon urundeuva [18
Germination positive apple [19
Dormancy alleviation (stratification) positive apple [20
Salt stress negative Arabidopsis [21
ABA cross-talk ABA positive regulator of rboh and ROS Arabidopsis [22
Cd Stress negative Arabidopsis [23
Mitochondrial functionning positive Arabidopsis [24
Salt stress positive Arabidopsis [25
Seed dormancy and iron deficiency positive Arabidopsis [26
Germination/ABA negative Arabidopsis [27
Salt stress/ethylene negative Arabidopsis [28
Germination/light positive Arabidopsis [29
Dormancy positive Arabidopsis [30
Germination/ABA/AIA positive Arabidopsis [31
Germination ABA GA positive Arabidopsis [32
Germination/ABA signalling positive Arabidopsis [33
Dormancy ABA GA positive barley [34
Seed germination and dormancy positive barley [35
Germination/ABA signalling positive barley [36
Dormancy alleviation positive barley [37
Germination/GA/NADPH oxidase positive barley [38
Germination/NADPH oxidase positive barley [39
Dormancy positive Bidens pilosa [40
Dormancy alleviation (stratification) positive Bunium persicum [41
Dormancy alleviation (stratification) positive Hedysarum scoparium [42
Germination/endosperm weakening positive lettuce [43
Mutagen agents negative maize [44
Dormancy alleviation by heat positive Mesembryanthemum crystallinum [45
Drought and salt stress negative Miscanthus [46
Germination/ABA positive pea [47
Germination positive Pea [48
High temperature, drought stress negative rice [49
Low phytic acid seed vigour positive rice [50
Dormancy alleviation (after-ripening) positive rice [51
Germination/NADPH oxidase positive rice [52
Osmotic and salt stress negative rice [53
Germination/ABA/GA positive rice [54
Germination/ethylene positive soybean [55
Dormancy alleviation (after ripening) positive sunflower [56
Dormancy alleviation/ABA/ethylene positive sunflower [57
Dormancy/after-ripening positive sunflower [11
Dormancy positive sunflower [58
GA response positive tobacco [59
Germination positive Vigna radiata [60
Germination positive Vigna radiata [61
Seed vigour and GA signalling positive watermelon [62
Dormancy positive wheat [63

These studies confirm and validate the concept of the oxidative window for germination [9]. In this concept the ability of a seed to germinate is directly dependent on ROS homeostasis: seed germination is likely to occur only when the seed ROS content is enclosed within values that allows ROS signalling but not ROS damage. In contrast, germination is thus prevented when the amount of ROS is too low or too elevated. Although there are no more doubts about the involvement of ROS in germination, many questions about their production and mode of action remain unsolved.

ROS production in seeds

Orthodox seeds, which undergo a dramatic desiccation phase at the end of their developmental program on planta, can survive for years in a resting and anhydrobiotic state. In this quiescent and desiccated state, major physiological changes such as dormancy alleviation or ageing are likely to occur. Seeds also endure an abrupt and invasive water uptake during their imbibition during which their moisture content can rapidly drop from values below 8–10% dry weight basis (dwb) to values higher than 50% dwb at the onset of radicle protrusion. Seed life plasticity has marked consequences on metabolism which is almost at a standstill in dry mature seeds and which is rapidly reactivated upon imbibition. This almost unique feature of metabolism variation (which is nevertheless also found in other anhydrobiotes) is in consequence associated with marked changes in ROS production mechanisms.

ROS metabolism and production in dry seeds are rarely investigated experimentally because this is technically challenging (most available methods require to use water, and then to modify the initial seed status). The ‘fuel' for producing ROS in anhydrobiosis is oxygen. In its ground state (3O2) oxygen has two unpaired electrons with parallel spins [64] and its reduction gives rise to the various forms of ROS. In dry seeds, oxygen is likely to be present in void spaces which altogether constitute an air space network [65]. In addition, seed desiccation on the mother plant generates ROS thus creating an oxidative environment within tissues of the mature seed [7]. If oxygen is present, chemical (non-enzymatic) reactions of ROS production can proceed during seed storage. Lipids, in particular, are very prone to oxidation at low moisture content and can serve as a source of free radicals. Lipid oxidation is known to have a U-shaped relationship with water activity (aw) [66]. It is favoured at very low moisture contents (i.e. zone I of water sorption isotherms) but increasing moisture content decreases lipid oxidation because it eliminates pores and decreases oxygen exposure of lipids to oxygen. It was also proposed that solubility or sorption of molecular oxygen in dehydrated products is lowered as water content increases, which in consequence can lower the reaction rate by decreasing the effective oxygen concentration [66,67]. In addition, in low moisture systems, peroxidation of lipids can lead to reactions of proteins with lipid hydroperoxides, free radicals and peroxide breakdown products [66].

The occurrence of ROS production during seed dry after-ripening has been demonstrated either directly by measuring the change in ROS content (eg [11]) or by following oxidation of biomolecules within seeds [56,68,69]. For example, after-ripening of sunflower embryonic axes was accompanied by a shift in the thiol-based cellular redox environment towards more oxidizing conditions [56] and by oxidation of proteins [11] and mRNAs [68]. In barley, the ROS content in the embryo was not affected by after-ripening, while the antioxidant glutathione (GSH) was gradually converted to glutathione disulfide (GSSG) [34]. The key role of oxygen in seed dormancy release during dry storage has been recently demonstrated by Buijs et al. [70] who increased the internal partial pressure of oxygen within Arabidopsis seeds to accelerate dormancy release. Indirect evidence was also given by Bazin et al. [71] and Basbouss-Serhal et al. [72] who studied dormancy alleviation of sunflower and Arabidopsis seeds, respectively, in a wide range of temperature and relative humidities. Both demonstrated that at low moisture content (below 7% dwb) dormancy alleviation was associated with negative energy activation, as determined by Arrhenius plots. Negative activation energies suggest that the kinetics of a biological process increases when temperature decreases and it reveals non-enzymatic processes, related to ROS production and oxidation mechanisms [71] thus confirming the measured changes in ROS content during dry after-ripening.

ROS production in imbibed seeds is better characterized and has been reviewed previously [7]. The studies of Bazin et al. [71] and Basbouss-Serhal et al. [72] demonstrated that metabolic activity in seeds could resume when moisture content reached values as low as 10% dwb in sunflower and ca. 13% dwb in Arabidopsis. Kibinza et al. [14] also demonstrated that respiration in sunflower embryonic axes became effective at 10% moisture content. This suggests that the shift from non-enzymatic to enzymatic ROS production can occur after a small water uptake by the dry seeds. Commonly detected ROS in imbibed seeds are superoxide, hydrogen peroxide and hydroxyl radical (see Table 1). The absence of functional chloroplasts in seeds does not favour the production of singlet oxygen, although it has already been detected in germinating seeds but it was proposed as being arising from lipid peroxidation [73]. Thus, in imbibed seeds, ROS are probably mainly produced by mitochondria. It is assumed that 1–2% of oxygen used by this organelle generates superoxide anion at complexes I and II of the electron transfer chain, then giving hydrogen peroxide [74]. H2O2 can further react through Fenton reaction with reduced Fe2+ to produce ·OH [75]. However, if mitochondrial ROS play a role in seed germination, their production must be controlled and regulated. Interestingly Ma et al. [24] recently demonstrated that a mitochondrial matrix-localized heat shock protein could induce ROS via modulation of CytC/C1 in the mitochondrial electron transport chain in response to temperature. This suggests that mitochondrial ROS could play a role in the sensing of environmental factors, here the temperature, during the germination process. The other candidates often mentioned in the context of regulation of germination by ROS are NADPH oxidases. NADPH oxidases (NOXs), also known as respiratory burst oxidase homologues (RBOHs), are certainly the most-studied ROS-producing enzymes [76]. They transfer electrons across the plasma membrane from cytoplasmic NADPH to molecular oxygen to produce superoxide in the apoplast which is rapidly dismutated to H2O2. The activity of NADPH oxidases has been frequently proposed to be involved in ROS production during seed imbibition (eg [77,30,38,39,52]) and, similarly to other plant systems, NOXs could play a role in sensing environmental conditions favourable for germination.

Attention has also to be paid to the diverse sources of apoplastic ROS production, since apoplastic ROS can play a critical role in cell wall weakening which precedes cell elongation. The apoplastic copper-containing amine oxidases and polyamine oxidases catalyze deamination of di- and polyamines and produce H2O2 [78]. Oxalate oxidases (germins and germin-like proteins) catalyze the oxidation of oxalate to CO2 and H2O2 [79]. Peroxidases and quinone reductase also generate ROS [80,81]. Most of these enzymes have been frequently cited as being involved in the late phase of germination, at the onset of radicle protrusion.

ROS content does not only depend on ROS production systems but is also regulated by the efficiency of enzymatic and non-enzymatic antioxidant mechanisms (already reviewed in seeds by [7]). Changes in activities of superoxide dismutase, catalase and enzymes of the ascorbate-glutathione cycle have been widely investigated in the context of seed germination. To understand the role of these systems in the regulation of seed germination, one nevertheless has to distinguish between seed germination under favourable conditions from germination under stressful conditions. The literature does not give a clear picture of the role of antioxidant enzymes in favourable conditions since their activities have been reported to either increase [63,8284] or decrease [35] during seed germination. However, it has often been reported that activation of antioxidant systems is rather a late event in the germination process: antioxidant enzymes would be activated only when ROS level exceed a certain value, in order to maintain ROS homeostasis within the oxidative window for germination. This also means that, in favourable conditions of germination, the level of ROS would be rather controlled by ROS-generating mechanisms. When seeds are germinated in non-optimal conditions there is a positive correlation between ROS scavenging ability through antioxidant systems and germination rate. For example, among some recent studies, seed antioxidant enzyme activities have been demonstrated to increase in response to high temperature and drought stress [49,85], low temperature [86], salt stress [87,88] or mutagen agents [44]. In those cases, the early activation of antioxidant enzymes is necessary to prevent excessive ROS accumulation and related oxidative damage. In contrast, in the context of seed dormancy, activities of antioxidant enzymes have often been shown to be lower, or even impaired, in non-dormant seeds than in dormant seeds, whatever the species [58,30,36,51,33]. In this context, their reduced efficiency can participate, in association with increased ROS production mechanisms, in the accumulation of ROS involved in dormancy release. Altogether the data available suggest that ROS can translate environmental cues to signals in seeds, as suggested by the concept of oxidative window, and that the fine-tuning of their production helps the seed to make a decision to germinate or not. This most likely occurs through the interaction with hormone signalling pathways.

There remain many unanswered questions relating to the regulation of ROS production in time and space. For example, it has been proposed recently that ROS signal could autopropagate in plants, leading to the concept of ROS wave, where ROS could diffuse from cell to cell via RBOHD [89]. With regards to the functional morphology of seeds, where the elongation zone of the embryonic axis is located behind the meristematic area [90], we can hypothesize that localized ROS production is important for germination control. We have examined this hypothesis in germinating seeds, using cell imaging of ROS production (Figure 1). We show that there is a dynamic production of ROS along the embryonic axis in germinating seeds of Arabidopsis (Figure 1). At an early timepoint of germination (6 h) ROS are mostly located in the meristem area of the radicle (Figure 1A,D) and further imbibition progressively relocalizes the maximum area of ROS production in the elongating zone of the hypocotyl (Figure 1B,C,E,F), thus evidencing a ‘developmental wave’ of ROS production during the germination process. This suggests that specific cell territories, i.e. the meristem area, could sense environmental cues and initiate a ROS signal propagating along the embryonic axis which ultimately could lead to cell elongation in the hypocotyl area. This finding has to be considered with regards to the spatiotemporal cell expansion mechanisms, related to ABA and GA metabolism and signalling, involved in the seed to seedling transition in Arabidopsis [91] and who share some similarities with spatiotemporal ROS production. Similarly, at the cellular level, during the germination process, it has also been demonstrated that ROS were first localized in the cytoplasm, then in the nucleus and finally in the cell wall at the time cells elongate [30]. ROS may therefore have distinct roles during the germination process, ranging from interaction with cytoplasmic signalling pathways (early germination), oxidative regulation of gene expression within the nucleus (mid-germination) and cell wall weakening (late germination). A better understanding of the role(s) of ROS in germination will require paying attention to the spatial regulation of their homeostasis at the whole organ and at the subcellular level.

Dynamics of ROS production during Arabidopsis seed germination.

Figure 1.
Dynamics of ROS production during Arabidopsis seed germination.

(AC) ROS detection in the embryonic axis of non-dormant seeds after 6 (A), 16 (B) and 24 h (C) of imbibition at 25°C in the dark. (DF) fluorescence intensity along a line running from the radicle tip (rt) to the hypocotyl shootward region (h), as shown in AC, in seeds imbibed for 6 (D), 16 (E) and 24 h (F). Seeds were imbibed as described below then seed coat was removed and embryos were incubated in 20 mM potassium phosphate buffer (pH 6.0) containing 50 mM fluorescence using 5-(and-6)-chloromethyl-2′,7′-dichlorofluorescein diacetate (DCFH-DA) for 15 min at 20°C in the dark. Samples were rinsed for 15 min in the potassium phosphate buffer solution and ROS production was visualized by confocal microscopy using Leica TCS SP5 confocal microscope, as described in [57]. Fluorescence intensity was estimated using Image-J software.

Figure 1.
Dynamics of ROS production during Arabidopsis seed germination.

(AC) ROS detection in the embryonic axis of non-dormant seeds after 6 (A), 16 (B) and 24 h (C) of imbibition at 25°C in the dark. (DF) fluorescence intensity along a line running from the radicle tip (rt) to the hypocotyl shootward region (h), as shown in AC, in seeds imbibed for 6 (D), 16 (E) and 24 h (F). Seeds were imbibed as described below then seed coat was removed and embryos were incubated in 20 mM potassium phosphate buffer (pH 6.0) containing 50 mM fluorescence using 5-(and-6)-chloromethyl-2′,7′-dichlorofluorescein diacetate (DCFH-DA) for 15 min at 20°C in the dark. Samples were rinsed for 15 min in the potassium phosphate buffer solution and ROS production was visualized by confocal microscopy using Leica TCS SP5 confocal microscope, as described in [57]. Fluorescence intensity was estimated using Image-J software.

ROS signalling is mediated by direct oxidation of biomolecules

The signalling role of ROS must also be considered through their oxidative effect on a wide range of molecules. Indeed the strong reactivity of ROS makes possible their direct oxidative action on various cellular components which can in turn modify cell functioning and in consequence whole seed physiology.

Proteins and nucleic acids can be easily oxidized by ROS. The role of these processes have been described previously in details [92] and is only briefly evoked here. The amino acids Cys and Met are very sensitive to oxidation. The oxidation of thiol to disulfide, is a known redox regulation mechanism, the reduced form being regenerated by the glutaredoxin and thioredoxin (Trx) systems. Various studies, reviewed in [92], have shown that germination might be associated with protein thiol oxidation, probably in balance with reduction in low molecular mass thiol disulfides [63,93,94]. Besides oxidation of sulfur-containing amino acids, carbonylation is the most common oxidative and non-reversible protein modification. It can result in loss of function and even degradation of the carbonylated proteins. Extensive protein carbonylation has been evidenced during germination of Arabidopsis, pea and rice seeds [95,47,51], and it was mostly directed towards reserve proteins. The authors of these papers proposed that carbonylation can be important for the mobilization of seed storage proteins because it increases protein susceptibility towards proteolytic cleavage by 20S proteasome. In addition, it was shown that carbonylation was not randomly distributed among proteins which suggests that oxidation of specific proteins is likely to play a role in the completion of germination. This idea was confirmed by Oracz et al. [11] who compared carbonylation patterns of dormant and non-dormant sunflower seeds and who showed that carbonylation was directed towards negative regulators of germination. In rice, Zhang et al. [51] showed that HSP and LEA, 2 known positive regulators of dormancy, became carbonylated during germination.

RNAs are also very sensitive to non-enzymatic oxidation [92]. The presence of oxidized bases in mRNAs causes translation errors and produces truncated proteins [92]. Bazin et al. [68] and Gao et al. [69] demonstrated that specific oxidation of a subset of transcripts was a prerequisite for dormancy release of sunflower and wheat seeds, respectively. It seems therefore that one of the role of ROS is to trigger direct oxidation of negative regulators of germination, as proposed by [92].

ROS can directly interact with cell wall polysaccharides and promote cell elongation in germinating seeds. The hydroxyl radical, in particular, is considered as a plant cell wall loosening agent which can directly cleaves wall polysaccharides [96]. ·OH can be formed either enzymatically, through the activity of secreted class III haem-containing peroxidases, or by Fenton reaction involving a transition metal [78]. In endospermic seeds, it has been demonstrated that endosperm cap weakening by ROS is an important process for allowing the elongating radicle to penetrate through the endosperm cap [77,43,97]. Interestingly endospermic ROS production is inhibited by ABA and promoted by GA and ethylene [77], thus underlying again the close connexion between ROS and hormone signalling pathways. ROS have also been shown to be produced in cell walls of growing embryos, at the time of radicle protrusion [97], including for non-endospermic seed species [48]. Depending on the species, it has been proposed that cell wall peroxidases, NADPH oxidases or polyamine oxidases were involved in ROS production in the apoplast of elongating cells of the embryonic axis [77,98,43,99,52,100]. Independently of the mechanisms of production, there is growing evidence showing that apoplastic ROS production is necessary for initiating cell elongation in the growing radicle. Such features should also be considered with regards to the recent findings of Stamm et al. [91] who highlighted the role of GA in the spatiotemporal cell expansion mechanisms in Arabidopsis.

ROS cross-talk with germination signalling pathways

ROS signalling effect on germination cannot be considered as whole but must be regarded as a part of a complex signalling network. Germination and dormancy being tightly regulated by hormones [13] it is therefore highly relevant to estimate the role of ROS in the context of hormone signalling and metabolism. The relationship between ROS and the hormones involved in germination, i.e. mostly ABA and GA, is now well documented but needs to be considered from various angles. In one way, an increase in ROS content, which is beneficial for germination, is associated with alteration of synthesis and signalling of ABA, the hormone which represses germination. It has been demonstrated that H2O2 accumulation in germinating seeds was associated with ABA degradation probably through the activation of ABA-8-hydroxylase, an ABA catalytic enzyme [32,36,39,59,84] even though the direct oxidation of ABA cannot be excluded [57,101,102]. As ABA regulates germination by its antagonistic interaction with GA it is worth noting that ROS have been reported to stimulate GA biosynthesis through a transcriptional effect [34,38,39,59,84]. In consequence ROS homeostasis has a direct effect on the hormonal balance ABA/GA in the favour of GA which in turn induces germination. To get a complete view of the relationship ROS/hormones it is also necessary to consider the effect of hormones on ROS production and scavenging. Direct imbibition of seeds with ABA, the use of mutants altered in ABA synthesis or signalling and the comparison of dormant to non-dormant seeds have shown that ABA represses ROS production in seeds [29,33,33,41,57]. Conversely, GA treatment has been shown to induce ROS production [57,83]. The relationship between other hormones which are putatively playing a role in germination and dormancy is less documented. Ethylene is a gaseous plant hormone which stimulates the germination of dormant seeds of many species [103]. A synergic relationship between ROS and ethylene has been demonstrated in sunflower seeds, with ethylene triggering ROS production [57,58,103,104]. Even though other plant hormones are likely to play role in germination, their possible interaction with ROS is not yet understood.

In plants, ROS, and mostly H2O2, have been reported to interact with other signalling pathways [1,4,105]. For example, mitogen-activated protein kinases (MAPK) can be activated by H2O2 accumulation to relay ROS signals [106], sometimes in connexion with hormone signalling [107]. H2O2 and Ca2+ signalling pathways are closely linked and can act in concert to regulate the effect of plant hormones, such as the effect of ABA on stomatal closure in response to drought [1]. Many examples have also highlighted that the relationship between NO and H2O2 can influence various plant developmental and processes and responses to biotic and abiotic factors [108,109]. A set of transcription factors relay the ROS message to transcriptome reprograming [110]. Members of MYB, DREB, ZAT, bHLH, WRKY, bZIP and NAC families have been reported to be associated with ROS signalling in plants [1,111]. However all these interactions are poorly described in the context of seed germination, and among them only the relationship between ROS and NO has retain attention some years ago [112].

Changes in ROS homeostasis can induce changes in seed gene expression. In plants, the effect of ROS on transcriptomes has been studied using ROS-generating treatments or mutants altered in ROS scavenging/production [113]. A global meta-analysis of microarray data obtained in such conditions allowed the definition of transcriptional footprints and led to design a so-called ROS wheel, in which co-regulated genes in response to ROS are clustered together [114]. This approach is relevant as it reveals oxidative components in a biological process using transcriptomic data. As an example, we have performed this analysis using the data obtained by Basbouss-Serhal et al. [115]. In this study the authors have identified a set of transcripts which became specifically associated with polysomes (i.e. the translatome) during imbibition of dormant and non-dormant Arabidopsis seeds. Such transcripts are likely to be translated and the corresponding proteins may then play a role in germination or dormancy. We have used the ROS wheel to investigate the ROS signature at the level of the translatome during seed imbibition (Table 2). The ROS wheel reveals the occurrence of ROS metabolism in seed germination, either in dormant or non-dormant seeds. Many transcripts range within the cluster III- High Light Early, especially in dormant seeds. This former cluster consists of transcription profiles triggered by high light exposures [114] and its over representation can appear surprising, but this is the largest cluster of the ROS wheel (more than 400 genes) and it also includes genes of response to heat or to H2O2, for example. Nevertheless, the ROS wheel also allows the discrimination of dormant from non-dormant seeds. It is worth noting that it reveals the occurrence of retrograde signalling in non-dormant seeds only, a process in which ROS production in either chloroplasts or mitochondria controls nuclear gene expression. This is in agreement with the recent findings of Ma et al. [24] who showed the role of mitochondrial ROS production in the germination process. The extended use of ROS footprints should help to better assess the involvement of ROS in seed germination.

Table 2
mRNA abundance in the translatome of dormant and non-dormant Arabidopsis seeds compared with the clusters from the ROS wheel analysis of ROS responses [114]
ROS wheel clustersmRNAs specifically found in the translatome of
non-dormant seeds atdormant seeds at
16 h of imbibition24 h of imbibition16 h of imbibition24 h of imbibition
I-GUN retrograde 22 
II-HL late 
III-HL early 36 14 79 61 
IV-ROS cell culture 
V-ROS 
VI-1O2-UVB early 
VII-RBOHF 
VIII-ROS acclimation 
Total 63 20 94 76 
ROS wheel clustersmRNAs specifically found in the translatome of
non-dormant seeds atdormant seeds at
16 h of imbibition24 h of imbibition16 h of imbibition24 h of imbibition
I-GUN retrograde 22 
II-HL late 
III-HL early 36 14 79 61 
IV-ROS cell culture 
V-ROS 
VI-1O2-UVB early 
VII-RBOHF 
VIII-ROS acclimation 
Total 63 20 94 76 

GUN, genome uncoupled mutants (known plastid retrograde signalling components); HL Late, 3 to 8 h of high light exposure; HL Early, 30 min to 2 h high light exposure; ROS cell culture, mitochondrial electron transport/ATP synthase inhibitor or H2O2 treatment of cell cultures; ROS, direct application or indirect generation of ROS in plants; 1O2, exposure to singlet oxygen; UVB Early, 15 min to 1 h of UV-B exposure, RBOHF, responses in rbohF mutant background; ROS Acclimation, redox mutants leading to long-term ROS stress. Translatome data are from Basbouss-Serhal et al. [115]. Dormant and non-dormant seeds were imbibed for 16 and 24 h at 25°C in the darkness.

The effects of ROS on transcriptional reprogramming during seed germination has been poorly investigated to date. In sunflower, a microarray analysis showed that treatment of dormant seeds by methylviologen, a ROS-generating compound inducing dormancy release, modified the expression of 120 genes. Most of the identified transcripts were related to cell signalling components [57]. Interestingly genes down-regulated in methylviologen-treated seeds were involved in ABA signalling, thus suggesting an interaction between ROS and ABA signalling pathways at the transcriptional level.

Conclusions

The beneficial role of ROS in the regulation of seed germination is increasingly well established with the studies reviewed here. This relationship is not always easy to address since ROS can either favour or repress germination. Figure 2 summarizes the main findings and hypotheses presented in this review. We propose that spatiotemporal regulation of ROS production in the embryonic axis of imbibed seeds controls the ability to germinate. The 3 steps model presented in Figure 2 suggests that sensing of environmental conditions is detected in the meristem region and that controlled production of ROS triggers germination mechanisms, i.e. activation of GA signalling pathway and oxidation of negative regulators of germination. At this early time point, ROS homeostasis mostly depends upon production sources. The localized increase in ROS generates an unknown signal that can propagate along the embryonic axis and trigger cell elongation in the hypocotyl area, at the onset of radicle protrusion. At the time of late imbibition, antioxidant systems participate to the control of ROS homeostasis and ROS are generated within the apoplast to participate in cell wall loosening. Further studies are required to better understand how environmental factors can fine tune ROS production, how the oxidative signal is translated at the subcellular level and how it can propagate from cell to cell. It is clear that ROS and hormones act in concert to regulate seed germination but the bases of this cross-talk are far from being understood. It will be of a particular interest to consider the spatiotemporal ROS production with regards to the recently evidenced spatiotemporal mode of action of hormones in the germination process [91,116].

A spatiotemporal model explaining the signalling role of ROS in seed germination.

Figure 2.
A spatiotemporal model explaining the signalling role of ROS in seed germination.

1. At the beginning of imbibition, environmental conditions are perceived by the imbibed seed at the meristematic region where a limited ROS production occurs through mitochondria electron transfer chain and NADPH oxidase activity. It induces the oxidation of negative regulators of germination, activation of gibberellin (GA) signalling and inactivation of abscisic acid (ABA) signalling. 2. The oxidative signal is propagated along the embryonic axis to the hypocotyl area. 3. At the onset of radicle protrusion cells elongate in the hypocotyl region after cell wall loosening caused by ROS production and apoplastic ROS (aROS) generation in the cell wall. Superoxide dismutase (SOD), catalase (CAT) and glutathione reductase (GR) are activated to prevent excessive ROS accumulation. Germination can then proceed.

Figure 2.
A spatiotemporal model explaining the signalling role of ROS in seed germination.

1. At the beginning of imbibition, environmental conditions are perceived by the imbibed seed at the meristematic region where a limited ROS production occurs through mitochondria electron transfer chain and NADPH oxidase activity. It induces the oxidation of negative regulators of germination, activation of gibberellin (GA) signalling and inactivation of abscisic acid (ABA) signalling. 2. The oxidative signal is propagated along the embryonic axis to the hypocotyl area. 3. At the onset of radicle protrusion cells elongate in the hypocotyl region after cell wall loosening caused by ROS production and apoplastic ROS (aROS) generation in the cell wall. Superoxide dismutase (SOD), catalase (CAT) and glutathione reductase (GR) are activated to prevent excessive ROS accumulation. Germination can then proceed.

Abbreviations

     
  • ABA

    abscisic acid

  •  
  • GA

    gibberellins

  •  
  • MAPK

    mitogen-activated protein kinases

  •  
  • NOXs

    NADPH oxidases

  •  
  • RBOHs

    respiratory burst oxidase homologues

  •  
  • ROS

    reactive oxygen species

Acknowledgements

The author thanks Rana Jurdark and Huifang Yang for her help with confocal imaging, Maharajah Ponnaiah for his help with the ROS wheel and George W. Bassel for editing and critical reading of the manuscript.

Competing Interests

The Author declares that there are no competing interests associated with this manuscript.

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