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Plant Signal Behav. 2008 March; 3(3): 175–182.
PMCID: PMC2634111

Oxidative signaling in seed germination and dormancy


Reactive Oxygen Species (ROS) play a key role in various events of seed life. In orthodox seeds, ROS are produced from embryogenesis to germination, i.e., in metabolically active cells, but also in quiescent dry tissues during after ripening and storage, owing various mechanisms depending on the seed moisture content. Although ROS have been up to now widely considered as detrimental to seeds, recent advances in plant physiology signaling pathways has lead to reconsider their role. ROS accumulation can therefore be also beneficial for seed germination and seedling growth by regulating cellular growth, ensuring a protection against pathogens or controlling the cell redox status. ROS probably also act as a positive signal in seed dormancy release. They interact with abscisic acid and gibberellins transduction pathway and are likely to control numerous transcription factors and properties of specific protein through their carbonylation.

Key words: seed, dormancy, germination, reactive oxygen species, hormones


Reactive oxygen species (ROS) derivate from the reduction of oxygen which gives rise to superoxide (O2-.), hydrogen peroxide (H2O2), hydroxyl radical (HO.) and singlet oxygen (1O2). Several reviews have described the signaling roles of ROS in plants (see for example, refs. 1 and 2) and their role in plant growth and development is now well documented.3 For example, hydrogen peroxide have been involved in programmed cell death (PCD),46 somatic embryogenesis,7 response to wounding,8 root gravitropism9 and ABA-mediated stomatal closure.10,11 The roles of superoxide and other ROS in signaling pathways are so far less well described; however O2-. seems to play a role in cell death and plant defence response.1214 In seeds, ROS production has been considered for a long time as being very detrimental, since the works dealing with ROS were mainly focused on seed ageing or seed desiccation, two stressful situations which often lead to oxidative stress.15 Numerous recent works have nevertheless brought new lines of evidence showing that the role of ROS in seeds is not as unfavourable as it was considered previously. At the opposite, it now appears more and more clearly that ROS would play a key signaling role in the achievement of major events of seed life, such as germination or dormancy release. The aim of this review is to present the current knowledge about the signaling role of ROS in orthodox seed germination and dormancy. This is actually particularly relevant because recent progresses in proteomics and transcriptomics have allowed the seed scientists to considerably enlarge their knowledge of seed dormancy and germination mechanisms, but these formers have also to be considered as a part of a complex regulatory network in which ROS are key signaling actors.

ROS Production and Sensing in Seeds

One of the most remarkable features of orthodox seeds is that their moisture content and metabolism vary dramatically from development to the completion of germination. Seed moisture content (MC) is high at the early stages of seed development, i.e., during embryogenesis, a developmental stage which is accompanied by an intense metabolic activity resulting in cell division. During seed filling, i.e., accumulation of reserves within the embryo or its surrounding structures, a sufficient amount of water is necessary for enabling metabolite transport through vascular connexions from a production source. This stage is followed by a dramatic loss of water during the so-called desiccation or maturation drying phase which requires the implementation of cellular adaptative mechanisms, among which ROS scavenging plays a key role,15 for allowing seed survival.16 At shedding, orthodox seeds are therefore fully desiccated (seed moisture content is generally below 0.10 g H2O g dry weight (DW)) and quiescent, with a metabolic activity almost at a standstill.17 Subsequent seed rehydration then allows germination, providing that the environmental conditions are appropriate or that the seeds are not dormant.

These contrasted situations, with regards to the hydration of the tissues, have marked consequences in term of ROS production. In developing or germinating seeds, the active mitochondria is probably one of the major sources of ROS, generating superoxide, and subsequently H2O2.18,19 Approximately 2–3% of the oxygen used by the mitochondria results into superoxide and hydrogen peroxide production.20,21 Chloroplasts can also generate ROS in the beginning of seed development, but they rapidly become non functional. The peroxisomes produce O2-. and H2O2, and in seeds, glyoxysomes, a particular type of peroxisomes involved in mobilization of lipid reserves produce high amounts of hydrogen peroxide resulting from the activity of enzymes such as glycolate oxidase.22 Finally, NADPH oxidases of the plasma membrane, which transfer electrons from cytoplasmic NADPH to oxygen, are also a major other source of superoxide radicals, which subsequently dismutate to H2O2.23,24 In dry seeds, enzyme activities are hardly probable,16 although the existence of hydrated pockets has been suggested in dry tissues thus possibly allowing some metabolic activity in restricted cellular areas.25 Therefore, ROS production in dry seeds would probably result mainly from non enzymatic mechanisms, such as those of Amadori and Maillard26,27 and lipid peroxidation.28 Lipid peroxidation is even favored at very low MC.28 Non enzymatic oxidative processes have been extensively studied in food science because oxidative processes in manufactured products are involved in their shelf life. For example, it has been demonstrated that glasses, which are also likely to exist in dry seeds, do not prevent oxygen diffusion and autoxidation of lipids.2931 For ROS to act as cellular messenger, seeds must be endowed with a ROS removing system that tightly regulates their concentration. The ROS-scavengers in seeds have already been described elsewhere15 and are not discussed here.

The ROS signaling transduction pathway in plants, and therefore in seeds, from sensing to changes in gene expression, is not fully understood yet. Again, the changes in cell water content during seed life suggest that seeds may cope with several sensing mechanisms. In hydrated tissues, for example during germination, presence of free water and low cytoplasmic viscosity, would allow ROS to travel within the cell. Therefore, as suggested by Moller et al.,32 short-lived ROS, such as HO, would react with sensors closed to their production site, whereas long-lived ROS, such as H2O2, could reach targets far from their production site. The established mechanisms of ROS transduction pathway might therefore be available in these conditions. They include MAP kinase cascade activation, inhibition of phosphatases, activation of Ca2+ channels and Ca2+-binding proteins1,2 but none of them have been clearly investigated in seeds. Conversely, in dry quiescent seeds, the absence of free water and an elevated cytoplasm viscosity probably limit the diffusion of ROS. Two nonexclusive hypotheses may be proposed for explaining ROS sensing in the dry state. The first one suggests that ROS would be ”sensed“ and then participate to the regulation of cell signaling in the dry state. This implies that cells would contain restricted hydrated zones allowing some molecular mobility, which would in turn permit ROS to be involved in cell signaling in these areas. Secondly, ROS could accumulate during dry storage but would become actors of cell regulatory mechanisms only after seeds get imbibed. It has indeed already been demonstrated that hydration of seeds causes a release of free radicals from the trapped state.33

Seed Germination

Germination is the process which leads to the elongation of the embryonic axis from a seed, allowing subsequent seedling emergence.17 It consists in hydration of the quiescent seed (imbibition, phase I of the full process), and in the achievement of many metabolic and molecular events during the so called germination sensu stricto phase which occurs at a constant seed MC (phase II). Completion of the germination sensu stricto is the critical step of germination because it requires the activation of a complex regulatory system which is controlled by intrinsic (i.e., dormancy) and extrinsic (i.e.,environmental conditions, such as temperature, oxygen and water availability) factors. Many reports have shown that the transition from a quiescent seed to a metabolically active organism is associated with ROS generation, suggesting that it is a widespread phenomenon. Production of hydrogen peroxide has been demonstrated at the early imbibition period of seeds of soybean,21,34,35 radish,36 maize,37 sunflower,38 wheat,39 pea40 and tomato41 seeds. Nitric oxide (NO),42,43 hydroxyl radicals36 and superoxide radicals,3436 also accumulate during the germination of seeds of various species. However, the intracellular sources of ROS production are poorly documented. Presumably, most of the ROS produced should originate from mitochondria, since resumption of respiration in imbibed seeds might lead to electron leakage and increased production of ROS. However, the putative role of NADPH oxidase during germination is not known yet but should require attention regarding the various roles of this enzyme in various developmental processes. For example, Sarath et al.43 demonstrated recently that NADPH oxidase inhibition delayed germination of warm season grasses. Several hypotheses can be proposed to explain the beneficial role of ROS during germination.

Endosperm weakening.

In seeds of some species, such as tobacco, tomato, pepper, Lepidium or Arabidopsis, germination is constraint by the micropylar endosperm, which covers the radicle tip.4446 Germination can proceed if the mechanical resistance imposed by the endosperm decreases to such a level that radicle can protrude through the weakened tissues. This endosperm weakening is under the regulation of abscissic acid (ABA) and gibberellic acid (GA)44 and several hydrolases (mannanase, cellulase, glucanase) have been suspected to contribute to cell-wall loosening.25,47 There is an increasing bundle of evidence suggesting that ROS would play a key role in this phenomenon and it has been proposed that they would be involved in cell wall loosening in growing tissues.4850 Hydroxyl radicals have been shown to be present in the cell walls of growing organs50,51 and they can break down polysaccharides by an oxidative scission of backbone bonds.5254 Their production could result from NADPH oxidase activity and/or Fenton reaction.48,55,56 Chen and Schopfer57 also suggested that cell wall peroxidases would play a role in hydroxyl radical formation. Furthermore, it has also been proposed that ROS might control polar growth through their effect on calcium channels55,58 and Schopfer et al.59 and Kawano et al.60 suggested that auxin might promote cell growth through O2-. production and the subsequent generation of hydroxyl radicals. Based on these properties, and on the role of ROS in some physiological processes, such as fruit softening,61 it is tempting to propose ROS as being involved in endosperm weakening during germination. Morohashi41 demonstrated that a peroxidase activity developed in the tomato endosperm cap prior to radicle emergence. In a recent study, Müller et al.56 also proposed that germination of Lepidium seeds, which requires endosperm rupture, involves the cleavage of cell wall polymers by ROS. They showed that H2O2 reversed the inhibitory effect of ABA on endosperm rupture, underlining the cross talk between these two compounds.

Protection against pathogens.

It is well known that ROS production in plants may be used as a weapon against pathogens.23 ROS may be either directly toxic against pathogenic microorganisms62 or trigger hypersensitive reaction and programmed cell death at sites attacked by pathogens.4,24 Many diseases being soil borne, the germination and seedling emergence are critical steps with regards to putative pathogen infection. Germinating seeds of lupine produce an oxidative burst when inoculated with an avirulent pathogen.63 Therefore, the rise in intracellular ROS in germinating seeds might constitute a defense reaction against infection by microorganisms. Additionally, extracellular production of ROS, extruded from germinating seeds, might also play a role in limiting the spread of invading pathogens by inhibiting spore germination and bacterial growth.64 This hypothesis needs however additional evidence for being properly addressed.

Redox regulation.

Another attempt for explaining the possible role of ROS accumulation during germination was to study protein carbonylation, an irreversible oxidation process leading to a loss of function of the modified proteins. Although protein carbonylation is often associated with aging in animals, it was demonstrated to occur in high vigor germinating Arabidopsis seeds, yielding vigorous plants.65 Interestingly carbonylation was not randomly distributed among the protein pool but directed against specific proteins, such as reserve proteins, including cruciferin subunits for example. Carbonylation of reserve proteins would help in their mobilization during germination by increasing their susceptibility to proteolytic cleavage.65 Proteins involved in glycolysis/gluconeogenesis pathways also became carbonylated during germination which could provide reducing power through the pentose phosphate pathway. This former hypothesis is particularly relevant because germination have often been proposed to be regulated by the cellular redox status. Redox regulation mainly leads to an alteration in the activity of target proteins via thiol-disulfide exchange, and is controlled by cellular redox agents, such as thioredoxins or glutathione/glutaredoxin.66,67 The involvement of thioredoxins in germination, particularly demonstrated in cereal seeds, begins to be well characterized. Thioredoxin h has been shown to facilitate the reduction of intramolecular disulfide bonds, which would in turn promotes the degradation of reserve proteins and the activation of various proteases.68,69 During germination, ROS might have an effect on the level of the ROS scavengers thioredoxin or reduced glutathione, and thereby modulate the redox signaling of these compounds.70 Alternatively, various transcription factors have been shown to sense ROS via the formation of disulfides involving thioredoxin and glutaredoxin.67 However, as suggested by Foyer and Noctor,3 the exact role of the redox sensing agents is often difficult to establish precisely because they are involved concurrently in redox signalisation cascades and defense against ROS.

Aleurone layer programmed cell death.

ROS, especially H2O2, have also been implicated in aleurone programmed cell death (PCD) of cereal grains during germination and seedling establishment.4,71 Aleurone layer of germinating cereal grains synthesizes and secretes hydrolytic enzymes for sustaining seedling growth before undergoing PCD.72,73 Activation of lipid and respiratory metabolisms leads to ROS proliferation, which are mainly generated in the aleurone cell glyoxysomes and mitochondria.74 This process is tightly regulated by the hormonal balance. GA promotes germinative and post-germinative processes, while ABA inhibits them.73,75 Exogenous H2O2 induces cell death in GA- but not in ABA-treated cells, which is related to the differential ability of these tissues to scavenge H2O2. While the activity of ROS scavenging enzymes, such as CAT, APX and SOD, is down-regulated in GA-treated layers, it is maintained in ABA-treated cells,4 which suggests that the capacity to cope with ROS seems to be linked to PCD execution. It has been reported that a decline of glyoxysomal catalase precedes PCD in aleurone cells and may contribute to an increase in cellular oxidative stress.4,74 ROS may then damage DNA, proteins and membrane lipids resulting in the loss of protein functions and membrane integrity. Other factors seem to regulate PCD in aleurone cells. Thus, blue and UV-A light accelerate PCD of GA-treated aleurone protoplasts but can not induce it in ABA-treated protoplasts.76 NO donors, in contrast, delay the loss of CAT and SOD and may be an endogenous modulator of PCD in barley aleurone cells.77 Interestingly, Kranner et al.78 showed recently that PCD also occurs in whole seeds and that the half-cell reduction potential of glutathione was involved in its initiation thus underlying the role of oxidative signaling in this process.

Finally there is still a domain to be explored in future studies dealing with germination and ROS, which concerns the direct effect of these compounds on gene expression. Changes in gene expression during germination7981 or dormancy release8284 are actually becoming more documented. The effects of ROS, and more particularly H2O2 on transcriptome have also been widely studied.85,86 However, up to date, there is no information available establishing a direct link between the changes in ROS content and gene expression during germination.

Seed Dormancy

Seed dormancy may be defined as the property of a seed that prevents its germination in apparently favorable conditions.17,46,87 It is a poorly understood phenomenon, influenced by the genetic background of the species, the environmental conditions and the balance of ABA and GA. Dormancy may be related to the embryo itself or to its surrounding structures (i.e., seed coat) which leads to distinguish several classes of dormancy.46 As the aim of this review is to focus on the signaling role of ROS, we will only present results dealing about their putative involvement in embryo (i.e., physiological) dormancy. Depending on the species, release of dormancy may mainly occur during after-ripening (storage in dry conditions) or during cold or warm stratification (imbibition at low or warm temperatures).17,46,8790 In both cases dormancy alleviation is associated with a widening of the environmental conditions allowing seed germination. Additionally, several compounds, often belonging to plant hormones, are known to allow the germination of dormant seeds; they include for example gibberellins, ethylene or cyanide.

Seed after-ripening.

Seed after-ripening occurs at such low seed moisture contents (MC), generally less than 0.10 g H2O/g DW-1, that water is probably not available for biochemical reactions. However, under these drastic conditions, seeds undergo dormancy alleviation. Leubner-Metzger25 proposed that local hydrated pockets within cells or tissues of the dormant seeds would allow changes in gene expression in the dry state. ROS been playing a role in cellular signaling, Bailly15 suggested that these compounds could facilitate the shift from a dormant to a nondormant status in seeds. Indeed, it is known that ROS can accumulate during seed storage in the dry state, as previously mentioned.28,9193 Oracz et al.94 and El-Maarouf-Bouteau et al.95 demonstrated that there was a clear cut relationship between sunflower seed dormancy alleviation and accumulation of ROS and peroxidation products in cells of embryonic axes, thus suggesting that ROS might play a role of signal in dormancy alleviation. These authors showed that proteins were one of the targets of ROS, since a pool of them became specifically carbonylated during after-ripening. Among this pool, some storage proteins became oxidized suggesting that breaking of dormancy in the dry state would be associated with a preparation toward storage protein mobilization. Interestingly, specific protein carbonylation also appeared when imbibed dormant sunflower seeds were treated by a dormancy release compound such as cyanide. Conversely, methylviologen, a ROS generating compound, alleviated dormancy and also triggered specific protein oxidation. This emphasizes the role of ROS and protein oxidation as a putative general mechanism of dormancy breaking, which will have to be assessed with dormant seeds of other species.

These former data are the first showing that ROS play a role in seed dormancy alleviation through at least protein oxidation. Because ROS are also known for being associated to gene expression, the possibility that they could act at genome level during after-ripening may be proposed. Modification of the genetic programme associated with the transition from a dormant to a nondormant state has been described in few reports. Apparent gene expression was detected during after-ripening in Nicotiana tabacum,25 Nicotiana plumbaginifolia,82 Arabidopsis,83 barley84 and sunflower.95 During after-ripening, numerous genes are differentially accumulated in dormant and nondormant seeds. Many of the genes up-regulated in nondormant seeds are associated with protein synthesis, potentially controlling the completion of germination.82,83 A proteomic analysis comparing dormant and after-ripened Arabidopsis seeds have shown a specific differential accumulation of proteins suggesting that proteins potentially involved in seed germination can accumulate during after-ripening.96 Although these data show that transcriptional and translational events could be a component of dormancy loss process, they provide little evidence on how genes are acting and whether ROS act directly or indirectly on gene expression during dormancy alleviation. Furthermore, because many of the highly expressed genes in the dormant state are stress-related, it was proposed that ABA, stress and dormancy responses overlap at the transcriptome level.83

Hormones and the control of seed dormancy.

Dormancy maintenance and release depend mainly on intrinsic balance of ABA and GA. While dormancy maintenance depends on high ABA/GA ratios, dormancy release involves increase of GA biosynthesis and ABA degradation resulting in low ABA/GA ratios.83,97 GA has been described as an internal regulator involved in the induction of germination, whereas ABA is widely recognized as being the most important hormone involved in the establishment and maintenance of seed dormancy.43,87,98 ABA, which imposes dormancy, originates from the seed itself during seed development and de novo ABA biosynthesis has been reported during imbibition of dormant seeds.97101 Mutants altered in hormone biosynthesis or hormone response/signal transduction allowed to better understand the role of each hormone and the interaction between the different hormone pathways (reviewed in ref. 44). Indeed, ABA deficiency during seed development is associated with the absence of primary dormancy and ABA overproduction is associated with enhanced dormancy. During after-ripening, associated with dormancy release, decreases in ABA sensitivity and concomitant increase of sensitivity to GA have been reported. There are also antagonistic effects of ABA and ethylene on dormancy and germination. Ethylene may promote germination by interfering with the ABA action on seed dormancy and/or maintenance of dormancy.102 Ethylene is implicated in the promotion of germination of nondormant seeds of a wide range of species.103107 In some species, such as sunflower, ethylene can break seed dormancy.103 Several components of the ethylene signal transduction have been identified and their signaling pathway has been characterized.44,108 Ethylene receptors are normally blocked to repress ethylene response.109 Upon ethylene binding, the receptors become active which alleviates the repression on ethylene signal transduction and allows ethylene responses.110 Ethylene signal transduction mutant studies highlight the interaction between ABA and ethylene signaling suggesting that ethylene suppresses dormancy by inhibiting ABA action.44

There are therefore strong presumptions that interactions between ABA, GA, ethylene and other hormones like auxin or brassinosteroids and extensive cross-talk among their respective signaling pathways play a major role in seed dormancy and germination.111 One may nevertheless wonder what is the nature and extent of the overlap and cross-talk in hormone responses, and how the switch from a dominant hormone signaling pathway to another occurs during the transition from seed dormancy to germination. Signal molecules such as ROS could be good candidates in this process since the interaction between hormones and ROS in other developmentally controlled processes in plants has been reported (reviewed in ref. 112).

Among the possible interplay between ROS and plant hormones, the relationship between H2O2 and ABA appears as the most probable. On the one hand, there exists evidence suggesting that hydrogen peroxide alleviates seed dormancy. Exogenous H2O2 stimulates the germination of dormant seeds of barley,100,113,114 rice,115 apple116 and Zinnia elegans.117 As early as 1975, Hendricks and Taylorson118 showed that inhibition of catalase activity promoted the germination of dormant seeds of lettuce and pigweed. Oracz et al.94 demonstrated that cyanide, a compound releasing sunflower seed dormancy, triggered ROS accumulation and protein oxidation. On the other hand, H2O2 seems to have a role in cellular response to ABA at the level of the gene expression and by regulating ion movements in guard cells.10,119 Furthermore, in vitro biochemical studies revealed that H2O2 inactivates ABI1 and ABI2 type 2C protein phosphatase, enzymes that function in ABA signaling.120,121 Treatment of dormant barley seeds with hydrogen peroxide results in a decrease in endogenous ABA level100,114 and alleviation of apple embryo dormancy by cyanide induces a simultaneous increase in H2O2 level and decrease in ABA content.116

Ethylene and ROS signalling pathways seem also to share some common mechanisms. Stimulation of ethylene synthesis by environmental stresses, such as ozone, UV irradiation, and wounding, involve generation of reactive oxygen species.122 Interactions among salicylic acid (SA), jasmonic acid (JA) and ethylene have been also reported and found to modulate responses to ROS (reviewed in ref. 123). Furthermore, it was shown that ethylene receptor ETR1 plays an important role in guard cell ROS signaling and stomatal closure.124

Finally, interaction between GA signaling and ROS was demonstrated in stem elongation.125,126 Maya-Ampudia and Bernal-Lugo127 showed that GA3 modified the redox status of aleurone proteins during germination, a process which might be related to ROS accumulation.

These data give strong indications about the interaction between hormones and ROS but there is up to date few results clearly demonstrating their crosstalk in seed dormancy. However, there is a growing evidence of the overlap of hormone signaling and ROS regulation in seed germination as described below. Furthermore, emerging evidence suggests that hormone signaling pathways regulated by ABA, SA, JA and ethylene, as well as ROS signaling pathways, play key roles in the crosstalk between biotic and abiotic stress signaling.128 Whether hormones and ROS interact in seed dormancy release and during germination process is still unknown but highly credible.

NO, a putative key player in the control of seed dormancy.

NO, a gaseous free radical that can be generated from nitrates, has also been proposed to be involved in seed dormancy alleviation. It was proposed that NO played a role as an endogenous regulator of germination in Arabidopsis and barley.129 However, NO promoting germination can be blocked by sufficiently high concentrations of ABA.129 Recently Bethke et al.130 demonstrated that Arabidopsis aleurone cells responded to NO, with NO being upstream of GA in a signaling pathway leading to dormancy alleviation, by up-regulating GA3ox1 and GA3ox2, two genes involved in the biosynthesis of active GA in Arabidopsis seeds. Other nitrogen-containing molecules such as azides and hydroxylamines stimulate germination of dormant seeds probably via their metabolism to NO.118,131 The focal point of convergence of both NO and H2O2 could be the fact that azide and hydroxylamine are converted to NO in a reaction catalyzed by catalase in the presence of H2O2.132 In addition, the NO-activated MAPK in tobacco can also be activated by H2O2.133 NO and H2O2 are commonly present during various stresses as reported in bacterially-induced PCD in soybean and Arabidopsis.134,135 Increase of ROS during dormancy release could induce NO production which can act in addition with H2O2 in the same MAPK signaling pathway.

Stratification and light.

Seed dormancy is also broken, in many plant species, by cold stratification, a prechilling treatment of fully imbibed seeds. Mechanisms underlying the physiological changes during cold stratification are still unknown but seem to be tightly related to GA. In fact, cold and light responses are mediated, in part, by promoting GA biosynthesis via enhanced expression of GA3 oxidase in Arabidopsis (AtGA3ox).136140 Light has been described to stimulate germination and to terminate dormancy of many species.141143 In seeds with coat dormancy, it is thought that light and GA can both release (coat) dormancy and promote germination.44,144146 Exogenous nitrate can affect the requirement for light to promote Arabidopsis seed germination. Nitrate regime fed to the mother plant seems to influence the initial level of Arabidopsis seed dormancy147 and germination,148 probably by a decline in ABA content in imbibing seeds.97,149

Previous studies have also highlighted tight links between ROS, cold and light in other plant processes. It has been reported that light and particularly UVB radiation produce ROS such as superoxide, H2O2 and singlet oxygen.150154 A-H-Mackerness et al.155 indicated that ROS play a pivotal role as secondary messengers in a number of UVB signal transduction pathways among key regulators. Indeed, ROS and plant hormones, SA, JA and ethylene have been shown to be key regulators of gene expression in response to UVB exposure.122,155157 In plant responses to temperature stress, increase in ROS has been implicated. H2O2 has been specifically involved in low temperature responses in plant.158 As temperature and light are the major natural factors conditioning seed dormancy and germination, it has now to be determined if ROS is the signal linking environmental stimuli to the hormone signalisation.


Seed dormancy and germination are very complex phenomena which involve tightly controlled signaling pathways and molecular regulations. In addition to hormones, there are many signaling molecules such as ROS and NO that seem to play a role in this process, but whether these processes relies on an unique dominant signaling pathway or on the overlap of many is unknown. A putative model, based on the references cited in the text, in which hormones and ROS compete for seed dormancy release and germination might be particularly attractive (Fig. 1). We assume here that germination is accompanied by ROS release, that ABA inhibits ROS accumulation and that GA reverses this inhibition. The hypothesis shown (Fig. 1) postulates that ROS play a central role with hormones, and particularly ABA, in dormancy release and germination completion. In the dormant state, ABA signaling pathway is active and prevents germination. High amount of ABA may maintain high level of ROS scavenging enzymes leading to a low level of ROS during imbibition of dormant seeds. During after-ripening there is an accumulation of ROS by nonenzymatic ROS production. This accumulation might reduce ABA level and/or block ABA signalling, stimulate GA signaling, modify redox status and downstream events and alter protein function through oxidative modifications. Subsequent imibition of after-ripened seeds would therefore be associated with the completion of germination. Further experiments in this area, especially in the -omics science, are likely to be highly informative for getting a comprehensive view of germination and dormancy release controlling events.

Figure 1
Hypothetical model proposing a central role of ROS in seed dormancy release and germination. In dormant state, high amount of ABA induces an active signaling pathway involved in dormancy maintenance. Lower ABA concentration in nondormant seeds would be ...


moisture content
reactive oxygen species
dry weight
abscissic acid


Previously published online as a Plant Signaling & Behavior E-publication:


1. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004;9:490–498. [PubMed]
2. Apel K, Hirt H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol. 2004;55:373–399. [PubMed]
3. Foyer CH, Noctor G. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell. 2005;17:1866–1875. [PubMed]
4. Fath A, Bethke PC, Jones RL. Enzymes that scavenge reactive oxygen species are down-regulated prior to gibberellic acid-induced programmed cell death in barley aleurone. Plant Physiol. 2001;126:156–166. [PubMed]
5. de Jong AJ, Yakimova ET, Kapchina VM, Woltering EJ. A critical role for ethylene in hydrogen peroxide release during programmed cell death in tomato suspension cells. Planta. 2002;214:537–545. [PubMed]
6. Pellinen RI, Korhonen MS, Tauriainen AA, Palva ET, Kangasjärvi J. Hydrogen peroxide activates cell death and defense gene expression in birch. Plant Physiol. 2002;130:549–560. [PubMed]
7. Cui K, Xing G, Liu X, Xing G, Wang Y. Effect of hydrogen peroxide on somatic embryogenesis of Lycium barbarum L. Plant Sci. 1999;146:9–16.
8. Orozco-Cardenas ML, Narvaez-Vasquez J, Ryan CA. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell. 2001;13:179–191. [PubMed]
9. Joo JH, Bae YS, Lee JS. Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol. 2001;126:1055–1060. [PubMed]
10. Pei ZM, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature. 2000;406:731–734. [PubMed]
11. Zhang X, Zhang L, Dong F, Gao J, Galbraith D, Song CP. Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol. 2001;126:1438–1448. [PubMed]
12. Doke N, Miura Y, Sanchez LM, Kawakita K. Involvement of superoxide in signal transduction: Responses to attack by pathogens, physical and chemical shocks and UV irradiation. In: Foyer CH, Mullineaux P, editors. Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. Boca Raton: CRC Press; 1994. pp. 177–218.
13. Jabs T, Dietrich RA, Dangl JL. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science. 1996;27:1853–1856. [PubMed]
14. Wisniewski JP, Cornille P, Agnel JP, Montillet JL. The extensin multigene family responds differentially to superoxide or hydrogen peroxide in tomato cell cultures. FEBS Lett. 1999;447:264–268. [PubMed]
15. Bailly C. Active oxygen species and antioxidants in seed biology. Seed Sci Res. 2004;14:93–107.
16. Vertucci CW, Farrant JM. Acquisition and loss of desiccation tolerance. In: Kigel J, Galili G, editors. Seed Development and Germination. New York: Marcel Dekker; 1995. pp. 237–271.
17. Bewley JD, Black M. Physiology of development and germination. 2nd ed. New York: Plenum Press; 1994. Seeds.
18. Moller IM. Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Ann Rev Plant Physiol Plant Mol Biol. 2001;52:561–591. [PubMed]
19. Noctor G, De Paepe R, Foyer CH. Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci. 2007;12:125–134. [PubMed]
20. Chance B, Boveris A, Oshino N, Loschen G. The nature of catalase intermediate and its biological function. In: King TE, Mason HS, Morrison, editors. Oxidases and Related Redox Systems. Baltimore: University Park Press; 1973. pp. 350–353.
21. Puntarulo S, Sanchez RA, Boveris A. Hydrogen peroxide metabolism in soybean embryonic axes at the onset of germination. Plant Physiol. 1988;86:626–630. [PubMed]
22. Huang AHC, Trelease RN, Moore TS. Plant Peroxisomes. London: Academic Press; 1983.
23. Lamb C, Dixon RA. The oxidative burst in plant disease resistance. Ann Rev Plant Physiol Plant Mol Biol. 1997;48:251–275. [PubMed]
24. Grant JJ, Loake GJ. Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol. 2000;124:21–30. [PubMed]
25. Leubner-Metzger G. Beta-1,3-glucanase gene expression in low-hydrated seeds as a mechanism for dormancy release during tobacco after-ripening. Plant J. 2005;41:133–145. [PubMed]
26. Priestley DA. Implications for Seed Storage and Persistence in the Soil. Ithaca: Cornell University Press; 1986. Seed aging.
27. Sun WQ, Leopold AC. The Maillard reaction and oxidative stress during aging of soybean seeds. Physiol Plant. 1995;94:94–104.
28. McDonald MB. Seed deterioration: Physiology, repair and assessment. Seed Sci Tech. 1999;27:177–237.
29. Nelson KA, Labuza TP. Relationship between water and lipid oxidation rates: Water activity and glass transition theory. In: St Angelo AJ, editor. Lipid Oxidation in Foods. Washington DC: American Chemical Society; 1992. pp. 93–103.
30. Andersen AB, Risbo J, Andersen ML, Skibsted LH. Oxygen permeation through an oil-encapsulating glassy food matrix studied by ESR line broadering using a nitroxyl spin probe. Food Chem. 2000;70:499–508.
31. Andersen ML, Skibsted LH. Detection of early events in lipid oxidation by electron spin resonance spectroscopy. Eur J Lipid Sci Technol. 2002;104:65–68.
32. Moller IM, Jensen PE, Hansson A. Oxidative modifications to cellular components in plants. Ann Rev Plant Biol. 2007;58:459–481. [PubMed]
33. Priestley DA, Werner BG, Leopold AC, McBride MB. Organic free radical levels in seeds and pollen: The effects of hydration and aging. Physiol Plant. 1985;64:88–94.
34. Puntarulo S, Galleano M, Sanchez RA, Boveris A. Superoxide anion and hydrogen peroxide metabolism in soybean embryonic axes during germination. Biochim Biophys Acta. 1991;1074:277–283. [PubMed]
35. Gidrol X, Lin WS, Degousee N, Yip SF, Kush A. Accumulation of reactive oxygen species and oxidation of cytokinin in germinating soybean seeds. Eur J Biochem. 1994;224:21–28. [PubMed]
36. Schopfer P, Plachy C, Frahry G. Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid. Plant Physiol. 2001;125:1591–1602. [PubMed]
37. Hite DRC, Auh C, Scandalios JG. Catalase activity and hydrogen peroxide levels are inversely correlated in maize scutella during seed germination. Redox Rep. 1999;4:29–34. [PubMed]
38. Bailly C, Bogatek-Leszczynska R, Côme D, Corbineau F. Changes in activities of antioxidant enzymes and lipoxygenase during growth of sunflower seedlings from seeds of different vigour. Seed Sci Res. 2002;12:47–55.
39. Caliskan M, Cuming AC. Spatial specificity of H2O2-generating oxalate oxidase gene expression during wheat embryo germination. Plant J. 1998;15:165–171. [PubMed]
40. Wojtyla L, Garnczarska M, Zalewski T, Bednarski W, Ratajczak L, Jurga S. A comparative study of water distribution, free radical production and activation of antioxidative metabolism in germinating pea seeds. J Plant Physiol. 2006;163:1207–1220. [PubMed]
41. Morohashi Y. Peroxidase activity develops in the micropylar endosperm of tomato seeds prior to radicle protrusion. J Exp Bot. 2002;53:1643–1650. [PubMed]
42. Caro A, Puntarulo S. Nitric oxide generation by soybean embryonic axes. Possible effect on mitochondrial function. Free Rad Res. 1999;31:S205–S212. [PubMed]
43. Sarath G, Hou G, Baird LM, Mitchell RB. Reactive oxygen species, ABA and nitric oxide interactions on the germination of warm-season C(4)-grasses. Planta. 2007;226:697–708. [PubMed]
44. Kucera B, Cohn MA, Leubner-Metzger G. Plant hormone interactions during seed dormancy release and germination. Seed Science Res. 2005;15:281–307.
45. Müller K, Tintelnot S, Leubner-Metzger G. Endosperm-limited Brassicaceae seed germination: Abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thaliana. Plant Cell Physiol. 2006;47:864–877. [PubMed]
46. Finch-Savage WE, Leubner-Metzger G. Seed dormancy and the control of germination. New Phytol. 2006;171:501–523. [PubMed]
47. Bradford KJ, Chen F, Cooley MB, Dahal P, Downie B, Fukunaga KK, Gee OH, Gurusinghe S, Mella RA, Nonogaki H, Wu CT, Yang H, Yim KO. Gene expression prior to radicle emergence in imbibed tomato seeds. In: Black M, Bradford KJ, Vazquez-Ramos J, editors. Seed Biology: Advances and Applications. Wallingford: CABI Publishing; 2000. pp. 231–251.
48. Fry SC. Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals. Biochem J. 1998;332:507–515. [PubMed]
49. Potikha TS, Collins CC, Johnson DI, Delmer DP, Levine A. The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol. 1999;119:849–858. [PubMed]
50. Liszkay A, van der Zalm E, Schopfer P. Production of reactive oxygen intermediates (O(2)(.-), H(2)O(2), and (.)OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol. 2004;136:3114–3123. [PubMed]
51. Renew S, Heyno E, Schopfer P, Liszkay A. Sensitive detection and localization of hydroxyl radical production in cucumber roots and Arabidopsis seedlings by spin trapping electron paramagnetic resonance spectroscopy. Plant J. 2005;44:342–347. [PubMed]
52. Fry SC, Dumville JC, Miller JG. Fingerprinting of polysaccharides attacked by hydroxyl radicals in vitro and in the cell walls of ripening pear fruit. Biochem J. 2001;357:729–737. [PubMed]
53. Schweikert C, Liszkay A, Schopfer P. Scission of polysaccharides by peroxidase-generated hydroxyl radicals. Phytochemistry. 2000;53:565–570. [PubMed]
54. Schweikert C, Liszkay A, Schopfer P. Polysaccharide degradation by Fenton reaction- or peroxidase-generated hydroxyl radicals in isolated plant cell walls. Phytochemistry. 2002;61:31–35. [PubMed]
55. Gapper C, Dolan L. Control of plant development by reactive oxygen species. Plant Physiol. 2006;141:341–345. [PubMed]
56. Müller K, Heß B, Leubner-Metzger G. A role for reactive oxygen species in endosperm weakening. In: Adkins S, Ashmore S, Navie S, editors. Seeds: Biology, Development and Ecology. Wallingford: CAB International; 2007. pp. 287–295.
57. Chen SX, Schopfer P. Hydroxyl-radical production in physiological reactions: A novel function of peroxidase. Eur J Biochem. 1999;260:726–735. [PubMed]
58. Carol RJ, Dolan L. The role of reactive oxygen species in cell growth: Lessons from root hairs. J Exp Bot. 2006;57:1829–1834. [PubMed]
59. Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A. Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta. 2002;214:821–828. [PubMed]
60. Kawano T. Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep. 2003;9:829–837. [PubMed]
61. Brummell DA, Dal Cin V, Lurie S, Crisosto CH, Labavitch JM. Cell wall metabolism during the development of chilling injury in cold-stored peach fruit: Association of mealiness with arrested disassembly of cell wall pectins. J Exp Bot. 2004;55:2041–2052. [PubMed]
62. De Rafael MA, Valle T, Babiano MJ, Corchete P. Correlation of resistance and H2O2 production in Ulmus pumila and Ulmus campestris cell suspension cultures inoculated with Ophiostoma novo-ulmi. Physiol Plant. 2001;111:512–518. [PubMed]
63. Morkunas I, Bednarski W, Kozlowska M. Response of embryo axes of germinating seeds of yellow lupine to Fusarium oxysporum. Plant Physiol Biochem. 2004;42:493–499. [PubMed]
64. Murphy TM, Asard H, Cross AR. Possible sources of reactive oxygen during the oxidative burst in plants. In: Asard H, Berczi A, editors. Plasma Membrane Redox Systems and their Role in Biological Stresses and Disease. Dordrecht: Kluwer Academic Publishers; 1998. pp. 215–246.
65. Job C, Rajjou L, Lovigny Y, Belghazi M, Job D. Patterns of protein oxidation in Arabidopsis seeds and during germination. Plant Physiol. 2005;138:790–802. [PubMed]
66. Foyer CH, Noctor G. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant. 2003;119:355–364.
67. Buchanan BB, Balmer Y. Redox regulation: A broadening horizon. Annu Rev Plant Biol. 2005;56:187–220. [PubMed]
68. Marx C, Wong JH, Buchanan BB. Thioredoxin and germinating barley: Targets and protein redox changes. Planta. 2003;216:454–460. [PubMed]
69. Wong JH, Cai N, Tanaka CK, Vensel WH, Hurkman WJ, Buchanan BB. Thioredoxin reduction alters the solubility of proteins of wheat starchy endosperm: An early event in cereal germination. Plant Cell Physiol. 2004;45:407–415. [PubMed]
70. Kranner I, Grill D. Significance of thiol-disulfide exchange in resting stages of plant development. Bot Act. 1996;109:8–14.
71. Fath A, Bethke P, Beligni V, Jones R. Active oxygen and cell death in cereal aleurone cells. J Exp Bot. 2002;53:1273–1282. [PubMed]
72. Jones RL, Jacobsen JV. Regulation of synthesis and transport of secreted proteins in cereal aleurone. Int Rev Cytol. 1991;126:49–88. [PubMed]
73. Bethke PC, Lonsdale JE, Fath A, Jones RL. Hormonally regulated programmed cell death in barley aleurone cells. Plant Cell. 1999;11:1033–1046. [PubMed]
74. Palma K, Kermode AR. Metabolism of hydrogen peroxide during reserve mobilization and programmed cell death of barley (Hordeum vulgare L.) aleurone layer cells. Free Radic Biol Med. 2003;35:1261–1270. [PubMed]
75. Wang M, Oppedijk BJ, Lu X, Van Duijn B, Schilperoort RA. Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Mol Biol. 1996;32:1125–1134. [PubMed]
76. Bethke PC, Jones RL. Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. Plant J. 2001;25:19–29. [PubMed]
77. Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL. Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol. 2002;129:1642–1650. [PubMed]
78. Kranner I, Birtic S, Anderson KM, Pritchard HW. Glutathione half-cell reduction potential: A universal stress marker and modulator of programmed cell death? Free Radic Biol Med. 2006;15:2155–2165. [PubMed]
79. de Diego JG, David Rodriguez F, Rodriguez Lorenzo JL, Grappin P, Cervantes E. cDNA-AFLP analysis of seed germination in Arabidopsis thaliana identifies transposons and new genomic sequences. J Plant Physiol. 2006;163:452–462. [PubMed]
80. Fait A, Angelovici R, Less H, Ohad I, Urbanczyk-Wochniak E, Fernie AR, Galili G. Arabidopsis seed development and germination is associated with temporally distinct metabolic switches. Plant Physiol. 2006;142:839–854. [PubMed]
81. Carrera E, Holman T, Medhurst A, Peer W, Schmuths H, Footitt S, Theodoulou FL, Holdsworth MJ. Gene expression profiling reveals defined functions of the ATP-binding cassette transporter COMATOSE late in phase II of germination. Plant Physiol. 2007;143:1669–1679. [PubMed]
82. Bove J, Lucas P, Godin B, Oge L, Jullien M, Grappin P. Gene expression analysis by cDNA-AFLP highlights a set of new signaling networks and translational control during seed dormancy breaking in Nicotiana plumbaginifolia. Plant Mol Biol. 2005;57:593–612. [PubMed]
83. Cadman CSC, Toorop PE, Hilhorst HWM, Finch-Savage WE. Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J. 2006;46:805–822. [PubMed]
84. Leymarie J, Bruneaux E, Gibot-Leclerc S, Corbineau F. Identification of transcripts potentially involved in barley seed germination and dormancy using cDNA-AFLP. J Exp Bot. 2007;58:425–437. [PubMed]
85. Desikan R, Mackerness SAH, Hancock JT, Neill SJ. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 2001;127:159–172. [PubMed]
86. Vandenabeele S, Van Der Kelen K, Dat J, Gadjev I, Boonefaes T, Morsa S, Rottiers P, Slooten L, Van Montagu M, Zabeau M, Inze D, Van Breusegem F. A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc Natl Acad Sci USA. 2003;100:16113–16118. [PubMed]
87. Bewley JD. Seed germination and dormancy. Plant Cell. 1997;9:1055–1066. [PubMed]
88. Baskin JM, Baskin CC. Seeds: Ecology, Biogeography and Evolution of Dormancy and Germination. San Diego, CA: Academic Press; 1998.
89. Koornneef M, Bentsink L, Hilhorst H. Seed dormancy and germination. Curr Opin Plant Biol. 2002;5:33–36. [PubMed]
90. Donohue K, Dorn L, Griffith C, Kim E, Aguilera A, Polisetty CR, Schmitt J. Niche construction through germination cueing: Life-history responses to timing of germination in Arabidopsis thaliana. Evolution. 2005;59:771–785. [PubMed]
91. Bucharov P, Gantcheff T. Influence of accelerated and natural aging on free radical levels in soybean seeds. Physiol Plant. 1984;60:53–56.
92. Hendry GAF. Oxygen free radical processes and seed longevity. Seed Sci Res. 1993;3:141–153.
93. Pukacka S, Ratajczak E. Production and scavenging of reactive oxygen species in Fagus sylvatica seeds during storage at varied temperature and humidity. J Plant Physiol. 2005;162:873–885. [PubMed]
94. Oracz K, El-Maarouf Bouteau H, Farrant JM, Cooper K, Belghazi M, Job C, Job D, Corbineau F, Bailly C. ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. Plant J. 2007;50:452–465. [PubMed]
95. El-Maarouf Bouteau H, Job C, Job D, Corbineau F, Bailly C. ROS signaling in seed dormancy alleviation. Plant Signal Behav. 2007;2:362–364. [PMC free article] [PubMed]
96. Chibani K, Ali-Rachedi S, Job C, Job D, Jullien M, Grappin P. proteomic analysis of seed dormancy in arabidopsis. Plant Physiol. 2006;142:1493–1510. [PubMed]
97. Ali-Rachedi S, Bouinot D, Wagner MH, Bonnet M, Sotta B, Grappin P, Jullien M. Changes in endogenous abscisic acid levels during dormancy release and maintenance of mature seeds: Studies with the Cape Verde Islands ecotype, the dormant model of Arabidopsis thaliana. Planta. 2004;219:479–488. [PubMed]
98. Koorneef M, Bentsink L, Hilhorst H. Seed dormancy and germination. Curr Opin Plant Biol. 2002;5:33–36. [PubMed]
99. Grappin P, Bouinot D, Sotta B, Miginiac E, Jullien M. Control of seed dormancy in Nicotiana plumbaginifolia: Post-imbibition abscisic acid synthesis imposes dormancy maintenance. Planta. 2000;210:279–285. [PubMed]
100. Wang M, Heimovaara-Dijkstra S, Van Duijn B. Modulation of germination of embryos isolated from dormant and nondormant barley grains by manipulation of endogenous abscisic levels. Planta. 1995;195:586–592.
101. Le Page-Degivry MT, Garello G. In situ abscisic acid synthesis: A requirement for induction of embryo dormancy in Helianthus annuus. Plant Physiol. 1992;98:1386–1390. [PubMed]
102. Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P. Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell. 2000;12:1117–1126. [PubMed]
103. Corbineau F, Bagniol S, Côme D. Sunflower (Helianthus annuus L.) seed dormancy and its regulation by ethylene. Israel J Bot. 1990;39:313–325.
104. Corbineau F, Côme D. Control of seed germination and dormancy by gaseous environment. In: Kigel J, Galili G, editors. Seed Development and Germination. New York: Marcel Dekker; 1993. pp. 397–427.
105. Kepczynski J, Kepczynska E. Ethylene in seed dormancy and germination. Physiol Plant. 1997;101:720–726.
106. Matilla AJ. Ethylene in seed formation and germination. Seed Science Res. 2000;10:111–126.
107. Leubner-Metzger G, Petruzzelli L, Waldvogel R, Vögeli-Lange R, Meins F., Jr Ethylene-responsive element binding protein (EREBP) expression and the transcriptional regulation of class I β-1,3-glucanase during tobacco seed germination. Plant Mol Biol. 1998;38:785–795. [PubMed]
108. Schaller GE, Keiber JJ. Ethylene. In: Somereville CR, Meyerowitz EM, editors. The Arabidopsis book. Rockville, MD: American Society of Plant Biologists; 2000. pp. 1–20.
109. Bleecker AB, Kende H. Ethylene: A gaseous signal molecule in plants. Annu Rev Cell Dev Biol. 2000;16:1–18. [PubMed]
110. Gamble RL, Qu X, Schaller GE. Mutational analysis of the ethylene receptor ETR1. Role of histidine kinase domain in dominant ethylene insensitivity. Plant Physiol. 2002;128:1428–1438. [PubMed]
111. Finkelstein RR, Gampala SS, Rock CD. Abscisic acid signaling in seeds and seedlings. Plant Cell. 2002;14:S15–S45. [PubMed]
112. Kwak JM, Nguyen V, Schoeder JI. The role of reactive oxygen species in hormonal responses. Plant Physiol. 2006;141:323–329. [PubMed]
113. Fontaine O, Huault C, Pavis N, Billard JP. Dormancy breakage of Hordeum vulgare seeds: Effects of hydrogen peroxide and scarification on glutathione level and glutathione reductase activity. Plant Physiol Biochem. 1994;32:677–683.
114. Wang M, van der Meulen RM, Visser K, Van Schaik HP, Van Duijn B, de Boer AH. Effects of dormancy-breaking chemicals on ABA levels in barley grain embryos. Seed Sci Res. 1998;8:129–137.
115. Naredo MEB, Juliano AB, Lu BR, De Guzman F, Jackson MT. Responses to seed dormancy-breaking treatments in rice species (Oryza L.) Seed Sci Tech. 1998;26:675–689.
116. Bogatek R, Gawroska H, Oracz K. Involvement of oxidative stress and ABA in CN-mediated elimination of embryonic dormancy in apple. In: Nicolas G, Bradford KJ, Côme D, Pritchard HW, editors. The Biology of Seeds: Recent Research Advances. Wallingford: CABI Publishing; 2003. pp. 211–216.
117. Ogawa K, Iwabuchi M. A mechanism for promoting the germination of Zinnia elegans seeds by hydrogen peroxide. Plant Cell Physiol. 2001;42:286–291. [PubMed]
118. Hendricks SB, Taylorson RB. Breaking of seed dormancy by catalase inhibition. Proc Natl Acad Sci USA. 1975;72:306–309. [PubMed]
119. Guan LM, Zhao J, Scandalios JG. Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J. 2000;22:87–95. [PubMed]
120. Meinhard M, Grill E. Hydrogen peroxide is a regulator of ABI1, a protein phosphatase 2C from Arabidopsis. FEBS Lett. 2001;508:443–446. [PubMed]
121. Meinhard M, Rodriguez PL, Grill E. The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta. 2002;214:775–782. [PubMed]
122. Surplus SL, Jordan BR, Murphy AM, Carr JP, Thomas B, Mackerness SAH. Ultraviolet-B-induced responses in Arabidopsis thaliana: Role of salicylic acid and reactive oxygen species in the regulation of transcripts encoding photosynthetic and acidic pathogenesis-related proteins. Plant Cell Environ. 1998;21:685–694.
123. Wang KLC, Li H, Ecker JR. Ethylene biosynthesis and signaling networks. Plant Cell. 2002;14:S131–S151. [PubMed]
124. Desikan R, Hancock JT, Bright J, Harrison J, Weir I, Hooley R, Neill SJ. A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells. Plant Physiol. 2005;137:831–834. [PubMed]
125. Shi L, Olszewski NE. Gibberellin and abscisic acid regulate GAST1 expression at the level of transcription. Plant Mol Biol. 1998;38:1053–1060. [PubMed]
126. Wigoda N, Ben-Nissan G, Granot D, Schwartz A, Weiss D. The gibberellin-induced, cysteine-rich protein GIP2 from Petunia hybrida exhibits in planta antioxidant activity. Plant J. 2006;48:796–805. [PubMed]
127. Maya-Ampudia V, Bernal-Lugo I. Redox-sensitive target detection in gibberellic acid-induced barley aleurone layer. Free Radic Biol Med. 2006;40:1362–1368. [PubMed]
128. Bethke PC, Gubler F, Jacobsen JV, Jones RL. Dormancy of Arabidopsis seeds and barley grains can be broken by nitric oxide. Planta. 2004;219:847–855. [PubMed]
129. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki Y, Shinozaki K. Crosstalk between abiotic and biotic stress responses: A current view from the points of convergence in the stress signaling networks. Curr Op Plant Biol. 2006;9:436–442. [PubMed]
130. Bethke PC, Libourel IG, Aoyama N, Chung YY, Still DW, Jones RL. The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol. 2007;143:1173–1188. [PubMed]
131. Taylorson RB, Hendricks SB. Dormancy in seeds. Annu Rev Plant Physiol. 1977;28:331–354.
132. Shahidullah M, Duncan A, Strachan PD, Rafique KM, Ball SL, McPate MJW, Nelli S, Martin W. Role of catalase in the smooth muscle relaxant actions of sodium azide and cyanamide. Eur J Pharmacol. 2002;435:93–101. [PubMed]
133. Samuel MA, Miles GP, Ellis BE. Ozone treatment rapidly activates MAP kinase signalling in plants. Plant J. 2000;22:367–376. [PubMed]
134. Delledonne M, Xia Y, Dixon RA, Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature. 1998;394:585–588. [PubMed]
135. Clarke A, Desikan R, Hurst RD, Hancock JT, Neill SJ. NO way back: Nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant J. 2000;24:667–677. [PubMed]
136. Yamaguchi S, Kamiya Y. Gibberellins and light-stimulated seed germination. J Plant Growth Reg. 2001;20:369–376. [PubMed]
137. Oh E, Kim J, Park E, Kim JI, Kang C, Choi G. PIL5, a phytochrome-interacting basic helix-loop-helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. Plant Cell. 2004;16:3045–3058. [PubMed]
138. Yamauchi Y, Ogawa M, Kuwahara A, Hanada A, Kamiya Y, Yamaguchi S. Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell. 2004;16:367–378. [PubMed]
139. Liu PP, Koizuka N, Homrichhausen TM, Hewitt JR, Martin RC, Nonogaki H. Large-scale screening of Arabidopsis enhancer-trap lines for seed germination-associated genes. Plant J. 2005;41:936–944. [PubMed]
140. Penfield S, Josse EM, Kannangara R, Gilday AD, Halliday KJ, Graham IA. Cold and light control seed germination through the bHLH transcription factor SPATULA. Curr Biol. 2005;15:1998–2006. [PubMed]
141. Vleeshouwers LM, Bouwmeester HJ, Karssen CM. Redefining seed dormancy: An attempt to integrate physiology and ecology. 1995;83:1031–1037.
142. Benech-Arnold RL, Sanchez RA, Forcella F, Kruk BC, Ghersa CM. Environmental control of dormancy in weed seed banks in soil. Field Crops Res. 2000;67:105–122.
143. Batlla D, Kruk BC, Benech-Arnold RL. Modelling changes in dormancy in weed soil seed banks: Implications for the prediction of weed emergence. In: Benech-Arnold RL, Sanchez RA, editors. Handbook of Seed Physiology: Applications to Agriculture. New York, NY: Food Product Press and the Haworth Reference Press; 2004. pp. 245–270.
144. Casal JJ, Sanchez RA. Phytochromes and seed germination. Seed Sci Res. 1998;8:317–329.
145. Leubner-Metzger G. Brassinosteroids and gibberellins promote tobacco seed germination by distinct pathways. Planta. 2001;2:758–763. [PubMed]
146. Sanchez RA, Mella RA. The exit from dormancy and the induction of germination: Physiological and molecular aspects. In: Benech-Arnold RL, Sanchez RA, editors. Handbook of Seed Physiology: Application to Agriculture. New York, NY: Food product Press and the Haworth Reference Press; 2004. pp. 221–243.
147. Aloresi A, Gestin C, Leydecker MT, Bedu M, Meyer C, Truong HN. Nitrate, a signal relieving seed dormancy in Arabidopsis. Plant Cell Env. 2005;28:500–512. [PubMed]
148. Batak I, Devic M, Giba Z, Grubisi D, Poff KL, Konjevic R. The effects of potassium nitrate and NO-donors on phytochrome A- and phytochrome B-specific induced germination of Arabidopsis thaliana seeds. Seed Sci Res. 2002;12:253–259.
149. Jacobsen JV, Pearce DW, Poole AT, Pharis RP, Mander LN. Abscisic acid, phaseic acid and giberellin contents associated with dormancy and germination in barley. Plant Physiol. 2002;115:428–441. [PubMed]
150. Andley UP, Clark BA. The effects of near-UV radiation on human lens b-crystallins: Protein structural changes and production of O2.- and H2O2. Photochem Photobiol. 1989;50:97–105. [PubMed]
151. Takeuchi Y, Kubo H, Kasahara H, Sasaki T. Adaptive alterations in the activities of scavengers of active oxygen in cucumber cotyledons irradiated with UV-B. J Plant Physiol. 1996;147:589–592.
152. Dai Q, Yan B, Huang S, Lin X, Peng S, Miranda MLM, Chavez AQ, Vergara BS, Olszyk D. Response of oxidative stress defense system in rice (Oryza sativa) leaves with supplemental UV-B radiation. Physiol Plant. 1997;101:301–308.
153. Hideg E, Mano J, Ohno C, Asada K. Increased levels of monodehydroascorbate radicals in UV-B-irradiated broad bean leaves. Plant Cell Physiol. 1997;38:684–690.
154. Kubo A, Aono M, Nakajima N, Saji H, Tanaka K, Kondo N. Differential responses in activity of antioxidant enzymes to different environmental stresses in Arabidopsis thaliana. J Plant Res. 1999;112:279–290.
155. A-H-Mackerness S, Surplus SL, Blake P, John CF, Buchanan- Wollaston V, Jordan BR, Thomas B. Ultraviolet-B induced stress and changes in gene expression in Arabidopsis thaliana: Role of signaling pathways controlled by jasmonic acid, ethylene and reactive oxygen species. Plant Cell Environ. 1999;22:1413–1424.
156. A-H-Mackerness S, Surplus SL, Jordan BR, Thomas B. Ultraviolet-B effects on transcript levels for photosynthetic genes are not mediated through carbohydrate metabolism. Plant Cell Environ. 1997;20:1431–1437.
157. Holley SR, Yalamanchili RD, Moura DS, Ryan CA, Stratmann JW. Convergence of signaling pathways induced by systemin, oligosaccharide elicitors, and ultraviolet-B radiation at the level of mitogen-activated protein kinases in Lycopersicon peruvianum suspension-cultured cells. Plant Physiol. 2003;132:1728–1738. [PubMed]
158. Allan AC, Maddumage R, Simons JL, Neill SO, Ferguson IB. Heat-induced oxidative activity protects suspension-cultured plant cells from low temperature damage. Func Plant Biol. 2006;33:67–76.

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