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Free Radicals and Antioxidant System in Seed Biology

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Fadime Eryılmaz Pehlivan

Submitted: March 20th, 2017 Reviewed: September 5th, 2017 Published: December 6th, 2017

DOI: 10.5772/intechopen.70837

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Reactive oxygen species (ROS) are involved in various development stages of seed biology. During seed desiccation, germination and aging, oxidative stress may increase in higher levels, leading to cellular damage and seed deterioration. Plant cells have antioxidant system, detoxifying enzymes and antioxidant compounds, that scavenge ROS, participating in seed survival. This antioxidant system has various roles in desiccation and germination of developing seeds, seed storability, and seed aging. On the other hand, ROS are accepted as molecules involving in cellular signaling, and having regulatory functions in seed development. ROS are also found to have roles in gene expression in early embryogenesis, dormancy and germination. Abscisic acid is a plant hormone and a signaling molecule in seed development and that is reported to have relationships with ROS. The objective of this article is to review the roles of ROS and the importance of antioxidant system in orthodox seeds, and to emphasize the dual effects of ROS in seed biology.


  • free radicals
  • reactive oxygen species (ROS)
  • antioxidant
  • seed biology
  • ROS signaling

1. Introduction

ROS are usually thought as hazardous molecules, attacking to biomolecules, leading to membrane and DNA injuries, and deleterious effects in seed germination processes [15]. Seed aging is a process that the roles of ROS are well documented [69]. ROS also have damages in desiccation of seeds by dehydration [10, 11]. Although ROS have been considered as detrimental to seeds up to now [1216], recent advances in plant physiology signaling pathways have led to reconsider their role [1729]. ROS accumulation can therefore be also beneficial for seed germination and seedling growth by regulating cellular growth, providing a protection against pathogens, and controlling the cellular redox status [3033]. ROS are also proved to act as a positive signal in seed dormancy release [3033]. The dual function of ROS in plants depends on the levels of antioxidant compounds, and enzyme activities release [3438]. By this way, plants can eliminate potentially harmful ROS that is produced under stress conditions, or control ROS concentrations in order to regulate various signaling pathways [3438]. This dual function of ROS is a very interesting subject in seed physiology. Even though there is a huge progress in this field, and the dual functions of ROS are quite well documented in the literature, it should also be regarded from a different point of view. The involvement of ROS in seed filling processes is not well documented, and the mobility of ROS in seeds has not yet been documented, thus, more data is needed on roles of ROS in seed germination and development physiology. Under light of the increasing progress made in the understanding of mechanisms driven by ROS, the role of ROS in seed biology may need to be revisited. To date, many distinct roles for ROS, apart from their toxic effects, have been identified.


2. ROS and antioxidant system

Oxygen is an essential element for the life of aerobic organism but it may become toxic at higher concentrations. Oxygen molecule in its ground state is relatively unreactive; but its partial reduction gives rise to reactive oxygen species (ROS). ROS are highly reactive oxygen molecules consisting of free radicals. Free radicals are an atom or molecule having an unpaired electron which is extremely reactive, starting chain reactions that generate many more free radicals, that are capable of attacking the healthy cells, causing them to lose their structure and function [15]. Types of ROS include the hydroxyl radical, the superoxide anion radical, hydrogen peroxide, singlet oxygen, nitric oxide radical, hypochlorite radical, and various lipid peroxides [15] (Table 1). Reduction of oxygen leads to the formation of the superoxide radical (O2•−), which is a molecule with an uncoupled electron and can react with other molecules to stabilize its energy. Hydrogen peroxide (H2O2) result from the nonenzymatic reduction of O2•− in the presence of H+ ions, or from the action of catalase on O2•−. H2O2 has a strong oxidizing capacity, and its life span is longer than that of superoxide. H2O2 can also diffuse through membranes and therefore reach target molecules at some distance from its production site [15].

Free radicalsNonradicals
Superoxide, O2•–Hydrogen peroxide, H2O2
Hydroperoxyl, HO2Ozone, O3
Peroxyl, ROO·Singlet oxygen, 1O2 or 1Δg
Hydroxyl, ·OHHypochlorous acid, HOCl
Alkoxyl, RO·Peroxynitrite, ONOO

Table 1.

Main reactive oxygen species (ROS) [1].

The Haber-Weiss and Fenton reactions involve superoxide radicals and H2O2. In the presence of iron or other transition metals, O2•− and H2O2 lead to the formation of the hydroxyl radical, OH, the most aggressive form of ROS, including the radical derivatives of oxygen (O2•−, OH), and also the peroxyl, alkoxyl or hydroperoxyl radicals, which are named as free radicals. Free radicals contain one or more unpaired electrons, but they also include nonradical derivatives of oxygen such as H2O2 and singlet oxygen [2, 5]. These free radicals are highly toxic and electrically charged molecules, i.e., they have an unpaired electron which causes them to seek out and capture electrons from other substances in order to neutralize themselves, all are capable of reacting with membrane lipids, nucleic acids, proteins and enzymes, and other small molecules, resulting in cellular damage, thus generate oxidative stress in plants [15].

Plants have developed a wide range of defense strategies to combat with these free radicals and deactivate their harmful effects known as antioxidants. The evolution of efficient antioxidant systems has enabled plant cells to overcome ROS toxicity and to use these reactive species as signal transducers [4, 5]. Antioxidants have diverse physiological roles in plants, acting as a scavenging and deactivating agent against oxidation, and converting the radicals to less reactive species, even at relatively small concentrations. The antioxidative system copes up with the harmful free radicals both by enzymatic (superoxide dismutase (SOD), catalase (CAT), peroxidase (POX), ascorbate peroxidase (APX), glutathione reductase (GR), polyphenol oxidase (PPO), etc.), and by nonenzymatic (ascorbic acid (vitamin C); α-tocopherol, carotenes, flavonoids, polyphenolics, etc.) systems (Table 2). Under unfavorable conditions such as extreme oxidative stress, this antioxidant system scavenges the toxic radicals, and thus helps the plants to survive through such conditions [15].

EnzymaticNonenzymatic or low molecular weight
CatalaseGlutathione (GSH)
Superoxide dismutase (SOD)Ascorbic acid (vitamin C)
Ascorbate-glutathione cycle enzymesTocopherols (vitamin E)
PeroxidasesPolyphenols (flavonoids)
Peroxiredoxin (Prx)

Table 2.

Main plant antioxidants [2].


3. ROS production in seeds

In plants, transport chain of electrons toward oxygen can potentially generate ROS. Seeds represent a particular case in this regard. During germination, the seed metabolic activity vary dramatically, meanwhile the sources of ROS in seeds also vary considerably [13, 3945]. The mitochondrial respiratory chain is one of the major sources of ROS; electron leakage from the transport chain generates superoxide, and subsequently H2O2, by dismutation of the former. During germination, respiratory activity increased and production of ROS enhanced [6, 14, 46, 47]. Another source of ROS is peroxisomes. Peroxisomes divided into: glyoxysomes (oily seeds), peroxisomes of photosynthetic tissues, nodule peroxisomes (Fabaceae nodules) and gerontosomes (senescing tissues) [14, 27, 4650]. In glyoxysomes, lipid reserves of oily seeds are converted into sugars during the first stages of seedling development [4951]. During this lipid oxidation process H2O2 is produced. In peroxisomal matrix, xanthine is also oxidized into uric acid by xanthine oxidase resulting with the production of superoxide [4951]. Catalase (H2O2 eliminating enzyme) is localized in peroxisomes [4952]. Production of nitric oxide (NO), (a free radical and also an important cellular signaling compound in plants) also takes place in peroxisomes [48, 5154]. NADPH oxidases of the cell membrane are another sources of ROS in plants, these enzymes transfer electrons from cytoplasmic NADPH to oxygen, producing superoxide radical and its dismutating product H2O2. NADPH oxidases are increased during plant infections [28, 29], in plant growth processes [55], and under severe abiotic stress conditions [56]. Enhanced activity of NADPH oxidase is reported in ABA induced generation of ROS under water stress [57, 58]. During biotic stress cell wall peroxidases and amine oxidases are induced leading to the formation of H2O2 in the apoplast [59]. As a result, mitochondria and peroxisomes are the major sources of ROS in nonquiescent seeds, during seed development and germination. Aquaporins and peroxiporins (transmembrane proteins) are shown to play roles in the transport of H2O2 in vegetative tissues [56, 60], but the mobility of ROS in seeds has not yet been documented. Finally, lipid oxidation can generate ROS that could be trapped in seed tissues [16, 61].


4. The dual effect of ROS: from toxicity to signaling

4.1. Toxicity of ROS

The oxidative stress may cause damage to DNA resulting in cancer and aging [62], and the presence of reactive oxygen also may initiate a chain reaction at the cellular level resulting in damage to critical cell bio-molecules [6365]. The uncontrolled accumulation of ROS, particularly of OH is highly toxic for the cell. These radicals are highly toxic and thus generate oxidative stress in plants. ROS can react with the majority of biomolecules, thus resulting in oxidative stress that can become irreversible and cause cellular damage [15]. Many harmful effects of ROS on cellular macromolecules have been identified [15]. All are capable of reacting with membrane lipids, nucleic acids, proteins and enzymes, and other small molecules, resulting in cellular damage [15]. Lipid peroxidation, which is a free-radical chain process leading to the deterioration of polyunsaturated fatty acids (PUFAs), is the best known cellular hazard among these, and has been studied intensively in food science [66]. Lipid peroxidation is initiated by free-radical attack upon a lipid, that gives starting to a chain reaction, removing a hydrogen atom from another fatty acid chain to form a lipid hydroperoxide (LOOH) in a propagation step [67]. This process is likely to degrade PUFAs present in membranes or in reserve lipids of oily seeds. Beside membranes, nucleic acids and proteins are also potential targets of ROS [67]. The hydroxyl radical, OH, can damage both nuclear and organelle DNA directly, by having ability to attack deoxyribose, purines and pyrimidines [67, 68]. Enzymes can also be inactivated easily by ROS, by degrading amino acids [69, 70]. ROS can damage transport proteins, receptors and ion channels and then lead to extensive cellular dysfunction [15, 69, 70].


5. The roles of ROS: cell signaling

Cellular antioxidant mechanisms control ROS concentrations, rather than to eliminate them completely, suggesting that some ROS may act as signaling molecules [5, 3437, 46]. Although ROS have been considered as detrimental to seeds, advances in plant physiology evaluated them as messengers of various signal transduction pathways in plants. ROS are suggested as being beneficial for seed germination, seedling growth, protection against pathogens and controlling the cell redox status [2840]. H2O2 is shown to be involved in the tolerance to various abiotic stresses acting as a secondary messenger [71], in cellular defense mechanisms against pathogens [72]. H2O2 has also been identified in many processes in plants, including programmed cell death (PCD) [8, 73], somatic embryogenesis [17], root gravitropism [19], and ABA-mediated stomatal closure [20, 21], response to wounding [74]. Superoxide (O2−•) found to have roles in cell death and plant defense [24]. H2O2 also proved to have roles in protein phosphorylation through mitogen-activated protein kinase (MAP kinase) cascades [75, 76], calcium mobilization [77, 78], and regulation of gene expression [79, 80].


6. Control of ROS levels: detoxifying mechanisms

In plants and animals ROS are deactivated by antioxidants. These antioxidants act as an inhibitor of the process of oxidation, even at relatively small concentration and thus have diverse physiological roles [40]. Antioxidant constituents of plant materials act as radical scavengers, and convert the radicals to less reactive species [81, 82]. Plants have developed an array of defense strategies (antioxidant system) to cope up with oxidative stress. Plant cells are equipped with mechanisms allowing scavenging (in the case of oxidative stresses) or homeostasis of ROS (for cellular signaling) [83]. The antioxidative system includes both enzymatic and nonenzymatic systems. The nonenzymatic system includes ascorbic acid (vitamin C); α-tocopherol, carotenes, etc., and enzymic system include superoxide dismutase (SOD), Superoxide dismutase, which can be mitochondrial (MnSOD), cytosolic (Cu/ZnSOD) or chloroplastic (CuZnSOD, FeSOD), dismutates superoxide radicals into H2O2 and oxygen [84]. Hydrogen peroxide is eliminated by the action of catalase (CAT), which is located in glyoxysomes and peroxisomes [51]. The ascorbate-glutathione cycle (also called the Halliwell-Asada cycle) also takes part in H2O2 scavenging. Ascorbate peroxidase (APX), monodehydroascorbate reductase (MDAR), dehydroascorbate reductase (DHAR), and glutathione reductase (GR) are involved in this cycle (Figure 1), and are present in chloroplasts, the cytoplasm, mitochondria, peroxisomes and the apoplast. These enzymes also participate in the regeneration of the powerful antioxidants such as reduced glutathione (GSH), ascorbic acid (vitamin C), and α-tocopherol (vitamin E) (Figure 1). Glutathione an important water-soluble antioxidant and is synthesized from the amino acids glycine, glutamate, and cysteine, which directly scavenges ROS such as lipid peroxides, and also plays a vital role in xenobiotic detoxification [8588]. Research suggests that glutathione and vitamin C work interactively to quench free radicals and that they have a sparing effect upon each other [8587]. Glutathione peroxidases (GPX) may also catalyze the reduction of H2O2 and hydroperoxides [8588]. Polyphenol oxidase (PPO), the function of this antioxidant system is to scavenge the toxic radicals produced during oxidative stress and thus help the plants to survive through such conditions. Various compounds, such as polyphenols, flavonoids and peroxiredoxins [89] also have a strong antioxidant function.

Figure 1.

Main detoxifying mechanisms in plants. CAT, catalase; SOD, superoxide dismutase; APX, ascorbate peroxidase; MDHAR, monodehydroascorbate reductase; DHAR, dehydroascorbate reductase; GR, glutathione reductase; ASA, ascorbate; MDHA, monodehydroascorbate; DHA, dehydroascorbate; GSSG, oxidized glutathione; GSH, reduced glutathione; α-tocH, α-tocopherol; α-toc, α-tocopheryl; LOOH, lipid peroxide; LOO, lipid radical (Halliwell-Asada cycle).


7. ROS and seed development

Seed development consists of embryogenesis, reserve accumulation and maturation/drying on the mother plant, leading from a zygotic embryo to a mature, quiescent seed. During maturation seeds undergo a period of desiccation where water content is reduced and the embryo is at a state of quiescence [10]. ROS are involved in final stage of seed development, in desiccation in tolerance. A dramatic loss of water becomes during desiccation or maturation phase which requires cellular adaptative mechanisms, at this stage ROS scavenging plays a key role, for allowing seed survival [10]. Recently, LEA (late embryogenesis abundant)-related proteins which are cited as accumulating proteins during drought conditions are correlated with desiccation tolerance, but their biological functions remain unclear [90]. A group-2 LEA class of proteins has been suggested to act as free-radical scavengers [91], emphasizing the importance of ROS scavenging in dehydration tolerance mechanisms. In developing or germinating seeds, the active mitochondria are probably one of the major sources of ROS, generating superoxide, and subsequently H2O2 [14, 32]. ROS is also generated in chloroplasts in the beginning of seed development, but they rapidly become nonfunctional [15, 63]. O2•− and H2O2 are produced in peroxisomes, and in seeds, glyoxysomes, which is a particular type of peroxisomes involving in mobilization of lipid reserves [15, 63]. High amounts of H2O2 are produced in glyoxysomes resulting from the activity of enzymes such as glycolate oxidase. H2O2 is known to promote seed germination of cereal plants, and exogenously applied H2O2 is shown to ameliorate seed germination in many plants [7, 92]. Ascorbic acid is the most important reducing substrate for removal of H2O2, acting as an antioxidant, in plant cells. It is reported that ascorbic acid suppresses the germination of wheat seeds, recently [93]. In plant cells, ascorbate peroxidase (APX) and catalase (CAT) that are involved in scavenging H2O2 are localized at the site of H2O2 generation [93] (Figure 2). H2O2 is mentioned to induce expression of many genes, coding defense-related proteins, transcription factors, phosphatases, kinases and enzymes involving in ROS synthesis or degradation [37, 54, 56, 79, 80] (Figure 2).

Figure 2.

Production and functions of H2O2 in seed biology [37].

Seed filling is also associated with the high potential of the H2O2 detoxification machinery, mainly due to APX and CAT activities [94]. It is suggested that cellular membranes in germinating tissues are vulnerable to damage from desiccation [10, 69]. After the loss of desiccation tolerance several products of peroxidized lipids are accumulated [45], and activated forms of oxygen are generated through xanthine oxidase [35, 48, 50]. Some studies have also suggested that ROS metabolism might also be important during initial embryogenesis [17, 95]. During embriogenesis, metabolic activity and mitochondrial respiration are increased, suggesting that developing embryos have the potential to generate significant amounts of ROS [17, 95]. The antioxidant ascorbate system reported to play an important role in embryogenesis and cell growth [41, 85]. Ascorbate content proposed to influence cell growth by modulating the expression of genes involved in hormonal signaling pathways [96]. Totipotency also related to antioxidant system, because of high ROS content and repressed expression of totipotency [97]. Conversely, ROS have beneficial effects in growth and development of plants. Seed germination requires release from dormancy. Treatment of dormant seeds with methylviologen (as a generator of ROS including OH) is reported to break dormancy [98]. Hydroxyl radicals are also postulated to be involved in cell wall extension during cell growth, and auxin-induced increases in OH production is speculated to be involved in cell wall elongation, stiffening, and lignification depending on the concentration of auxin [55, 99]. Hydrogen peroxide is suggested to participate in lignin deposition in the cell walls in a peroxidase-catalyzed reaction [100]. The involvement of a diamine oxidase in H2O2 production has been demonstrated along with lignin deposition in the chalazal cells, in developing barley grains, in developing barley grains [100]. Production of ROS and their release in the surrounding medium are supposed to play a part in protecting the embryo against pathogens during seed imbibition [99]. Some of the selected published reviews on the dual roles of ROS in seed biology are listed in Table 3.

ROS moleculePhysiological traitReference
Hydrogen peroxide (H2O2)Alleviation of seed dormancyWang et al. [104]
H2O2Somatic embryogenesisCui et al. [17]
Superoxide (O2)Plant defense responseWisniewski et al. [24]
O2Survival and germination seedsRoach et al. [105]
H2O2Response to woundingOroczo-Cardenas et al. [74]
H2O2Seed germination-ABA levelsBarba-Espin et al. [102]
Hydroxyl radical (OH)Breakdown of polysaccharidesSchweikert et al. [106]
O2Cell growth by auxinSchopfer et al. [55]
OHCell wall looseningMüller et al. [107]
H2O2Lateral root formationChen et al. [101]
H2O2Seed germination via pentose phosphate pathwayBarba-Espin et al. [103]
H2O2Programmed cell deathde Jong et al. [8]
O2Cell deathDoke et al. [22]

Table 3.

Published reviews on the dual role of ROS in seed physiology [34].

As shown above, the effects of ROS, and more particularly H2O2 on transcriptome have been widely studied [56]. However, up to date, there is no information available establishing a direct link between the changes in ROS content and gene expression during seed germination and development. Further experiments in this area, will be highly informative for getting a comprehensive view of ROS in seed biology.


8. Conclusion

ROS and antioxidants play important roles in seed biology. In seed life, ROS are involved in all the stages of seed development, from embryogenesis to germination. ROS can react with the majority of biomolecules, resulting in cellular damage. In developing or germinating seeds, major amounts of ROS are generated, which are highly toxic and thus generate oxidative stress in seed cells. Plants have developed an array of defense strategies (antioxidant system) to cope up with oxidative stress. Conversely, ROS are suggested to have beneficial effects in growth and development of seeds, and are considered as part of a signaling network involving in numerous regulatory components of seed development. For example, H2O2 is known to promote seed germination of cereal plants. The antioxidant system reported to play an important role in embryogenesis and cell growth. Ascorbate content is proposed to influence cell growth by modulating the expression of genes involved in hormonal signaling pathways. The above findings show that, these dual effects of ROS in seed biology are very interesting subjects and need further examinations for determination of the roles of ROS in seed physiology. Depending on the progress that has been required in seed tissue physiology, cellular production sites of ROS and their diffusion within the cell are established. Investigations in this field encourage to enlighten the cellular mechanisms involved in acquisition of the desiccation tolerance, germination and alleviation of dormancy. Finally, ROS signaling transduction pathway in seeds, from sensing to changes in gene expression, is not fully understood yet. Therefore, there is still a domain to be examined in future studies dealing with seed biology and ROS, which concerns the direct effects of these compounds on gene expression. Analyses of gene expression using the novel methods will be of help in elucidating the mechanisms underlying the interplay of ROS with hormones and their cross-talk in seed germination and development, providing a challenge for future research in this area.


  1. 1. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine. United Kingdom, Oxford University Press; 2007
  2. 2. Halliwell B. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiology. 2006;141:312-322
  3. 3. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends in Plant Science. 2004;9:490-498 [PubMed]
  4. 4. Apel K, Hirt H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology. 2004;55:373-399 [PubMed]
  5. 5. Foyer CH, Noctor G. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell. 2005;17:1866-1875 [PMC free article] [PubMed]
  6. 6. Sun WQ, Leopold AC. The Maillard reaction and oxidative stress during aging of soybean seeds. Physiologia Plantarum. 1995;94:94-104
  7. 7. 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 Physiology. 2001;126:156-166 [PMC free article] [PubMed]
  8. 8. 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]
  9. 9. Pellinen RI, Korhonen MS, Tauriainen AA, Palva ET, Kangasjärvi J. Hydrogen peroxide activates cell death and defense gene expression in birch. Plant Physiology. 2002;130:549-560 [PMC free article][PubMed]
  10. 10. Pammenter NW, Berjak P. A review of recalcitrant seed physiology in relation to desiccation tolerance mechanisms. Seed Science Research. 1999;9:13-37
  11. 11. 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. p. 237-271
  12. 12. Bailly C. Active oxygen species and antioxidants in seed biology. Seed Science Research. 2004;14:93-107
  13. 13. Bewley JD, Black M. Seeds Physiology of Development and Germination. 2nd ed. New York: Plenum Press; 1994
  14. 14. Moller IM. Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology. 2001;52:561-591 [PubMed]
  15. 15. Noctor G, De Paepe R, Foyer CH. Mitochondrial redox biology and homeostasis in plants. Trends in Plant Science. 2007;12:125-134 [PubMed]
  16. 16. McDonald MB. Seed deterioration: Physiology, repair and assessment. Seed Science and Technology. 1999;27:177-237
  17. 17. Cui K, Xing G, Liu X, Xing G, Wang Y. Effect of hydrogen peroxide on somatic embryogenesis of Lycium barbarum L. Plant Science. 1999;146:9-16
  18. 18. Buchanan BB, Balmer Y. Redox regulation: A broadening horizon. Annual Review of Plant Biology. 2005;56:187-220 [PubMed]
  19. 19. Joo JH, Bae YS, Lee JS. Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiology. 2001;126:1055-1060 [PMC free article] [PubMed]
  20. 20. 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]
  21. 21. 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 Physiology. 2001;126:1438-1448 [PMC free article][PubMed]
  22. 22. 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. p. 177-218
  23. 23. Jabs T, Dietrich RA, Dangl JL. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science. 1996;27:1853-1856 [PubMed]
  24. 24. Wisniewski JP, Cornille P, Agnel JP, Montillet JL. The extensin multigene family responds differentially to superoxide or hydrogen peroxide in tomato cell cultures. FEBS Letters. 1999;447:264-268 [PubMed]
  25. 25. 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. p. 350-353
  26. 26. Puntarulo S, Sanchez RA, Boveris A. Hydrogen peroxide metabolism in soybean embryonic axes at the onset of germination. Plant Physiology. 1988;86:626-630 [PMC free article] [PubMed]
  27. 27. Huang AHC, Trelease RN, Moore TS. Plant Peroxisomes. London: Academic Press; 1983
  28. 28. Lamb C, Dixon RA. The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology. 1997;48:251-275 [PubMed]
  29. 29. Grant JJ, Loake GJ. Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiology. 2000;124:21-30 [PMC free article] [PubMed]
  30. 30. Kucera B, Cohn MA, Leubner-Metzger G. Plant hormone interactions during seed dormancy release and germination. Seed Science Research. 2005;15:281-307
  31. 31. El-Maarouf-Bouteau H, Bailly C. Oxidative signaling in seed germination and dormancy. Plant Signaling & Behavior. 2008;3(3):175-182
  32. 32. 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 Physiology and Biochemistry. 1994;32:677-683
  33. 33. Hendricks SB, Taylorson RB. Breaking of seed dormancy by catalase inhibition. Proceedings of the National Academy of Sciences. 1975;72:306-309
  34. 34. Kumar SPJ, Prasad SR, Banerjee R, Thammineni C. Seed birth to death: Dual functions of reactive oxygen species in seed physiology. Annals of Botany. 2015;116:663-668
  35. 35. del Río LA. ROS and RNS in plant physiology: An overview. Journal of Experimental Botany. 2015;66(10):2827-2837
  36. 36. You J, Chan Z. ROS regulation during abiotic stress responses in crop plants. Frontiers in Plant Science. 2015;6:1-15
  37. 37. Wojtyla L, Lechowska K, Kubala S, Garnczarska M. Different modes of hydrogen peroxide action during seed germination. Frontiers in Plant Science. 2016;7:1-16
  38. 38. Barba-Espín G, Hernández JA, Diaz-Vivancos P. Role of H2O2 in pea seed germination. Plant Signaling & Behavior. 2012;7(2):193-195
  39. 39. Caliskan M, Cuming AC. Spatial specificity of H2O2-generating oxalate oxidase gene expression during wheat embryo germination. The Plant Journal. 1998;15:165-171 [PubMed]
  40. 40. Chien CT, Lin TP. Mechanism of hydrogen peroxide in improving the germination of Cinnamonum camphora seed. Seed Science and Technology. 1994;22:231-236
  41. 41. De Gara L, de Pinto MC, Arrigoni O. Ascorbate synthesis and ascorbate peroxidase activity during the early stage of wheat germination. Physiologia Plantarum. 1997;100:894-900
  42. 42. Hite DRC, Auh C, Scandalios JG. Catalase activity and hydrogen peroxide levels are inversely correlated in maize scutella during seed germination. Redox Report. 1999;4:29-34
  43. 43. Puntarulo S, Galleano M, Sanchez RA, Boveris A. Superoxide anion and hydrogen peroxide metabolism in soybean embryonic axes during germination. Biochimica et Biophysica Acta. 1991;1074:277-283 [PubMed]
  44. 44. Simontacchi M, Caro A, Fraga CG, Puntarulo S. Oxidative stress affects α-tocopherol content in soybean embryonic axes upon imbibition and following germination. Plant Physiology. 1993;103:949-953
  45. 45. Smith MT, Berjak P. Deteriorative changes associated with the loss of viability of stored desiccation tolerant and desiccation-sensitive seeds. In: Kigel J, Galili G, editors. Seed Development and Germination. New York: Marcel Dekker; 1995. p. 701-746
  46. 46. Foyer CH, Noctor G. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiologia Plantarum. 2003;119:355-364
  47. 47. Staniek K, Nohl H. Are mitochondria a permanent source of reactive oxygen species? Biochimica et Biophysica Acta. 2000;1460:268-275
  48. 48. Corpas FJ, Barroso JB, del Rio LA. Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends in Plant Science. 2001;6:145-150
  49. 49. Reumann S. The structural properties of plant peroxisomes and their metabolic significance. Biological Chemistry. 2000;381:639-648
  50. 50. del Rio LA, Pastori GM, Palma JM, Sandalio LM, Sevilla F, Corpas FJ, Jimenez A, Lopez-Huertas E, Hernandez JA. The activated oxygen role of peroxisomes in senescence. Plant Physiology. 1998;116:1195-1200
  51. 51. Willekens H, Inzé D, Van Montagu M, Van Camp W. Catalases in plants. Molecular Breeding. 1995;1:207-228
  52. 52. Kawano T. Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Reports. 2003;9:829-837 [PubMed]
  53. 53. Durner J, Klessig DF. Nitric oxide as a signal in plants. Current Opinion in Plant Biology. 1999;2:369-374
  54. 54. Neill SJ, Desikan R, Hancock JT. Nitric oxide signalling in plants. New Phytologist. 2003;159:11-35
  55. 55. 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]
  56. 56. Neill S, Desikan R, Hancock J. Hydrogen peroxide signalling. Current Opinion in Plant Biology. 2002;5:388-395
  57. 57. Jiang M, Zhang J. Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. Journal of Experimental Botany. 2002;53:2401-2410
  58. 58. Jiang M, Zhang J. Involvement of plasmamembrane NADPH oxidase in abscisic acid- and water stress-induced antioxidant defense in leaves of maize seedlings. Planta. 2002;215:1022-1030
  59. 59. Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F. The apoplastic oxidative burst in response to biotic stress in plants: A three-component system. Journal of Experimental Botany. 2002;53:1367-1376
  60. 60. Henzler T, Steudle E. Transport and metabolic degradation of hydrogen peroxide in Chara corallina: Model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. Journal of Experimental Botany. 2000;51:2053-2066
  61. 61. 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
  62. 62. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, van Breusegem F. ROS signaling: The new wave? Trends in Plant Science. 2011;16:300-309
  63. 63. Sung JM. Lipid peroxidation and peroxide scavenging in soybean seeds during aging. Physiologia Plantarum. 1996;97:85-89
  64. 64. Wilson DO, McDonald MB. The lipid peroxidation model of seed aging. Seed Science and Technology. 1986;14:269-300
  65. 65. Bailly C, Benamar A, Corbineau F, Côme D. Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seeds as related to deterioration during accelerated aging. Physiologia Plantarum. 1996;97:104-110
  66. 66. Beckman KB, Ames BN. Oxidants, antioxidants, and aging. In: Scandalios JG, editor. Oxidative Stress and the Molecular Biology of Antioxidant Defenses. New York: Cold Spring Harbor Laboratory Press; 1997. p. 201-246
  67. 67. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine. 3rd ed. New York: Oxford University Press; 1999
  68. 68. Chen SX, Schopfer P. Hydroxyl-radical production in physiological reactions: A novel function of peroxidase. European Journal of Biochemistry. 1999;260:726-735
  69. 69. Smirnoff N. The role of active oxygen in the response of plants to water deficit and desiccation. New Phytologist. 1993;125:27-58
  70. 70. Charles SA, Halliwell B. Effect of hydrogen peroxide on spinach (Spinacia oleracea) chloroplast fructose bisphosphatase. Biochemical Journal. 1980;189:373-376
  71. 71. Prasad TK, Anderson MD, Martin BA, Stewart CR. Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell. 1994;6:65-74
  72. 72. Levine A, Tenkanen R, Dixon R, Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994;79:583-593
  73. 73. Desikan R, Reynolds A, Hancock JT, Neill SJ. Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defence gene expression in Arabidopsis suspension cultures. Biochemical Journal. 1998;330:115-120
  74. 74. 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 [PMC free article] [PubMed]
  75. 75. Kovtun Y, Chiu WL, Tena G, Sheen J. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proceedings of the National Academy of Sciences. 2000;97:2940-2945
  76. 76. Samuel MA, Miles GP, Ellis BE. Ozone treatment rapidly activates MAP kinase signalling in plants. Plant Journal. 2000;22:367-376
  77. 77. Bowler C, Fluhr R. The role of calcium and activated oxygens as signals for controlling crosstolerance. Trends in Plant Science. 2000;5:241-246
  78. 78. Murata Y, Pei ZM, Mori IC, Schroeder J. Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2c mutants. Plant Cell. 2001;13:2513-2523
  79. 79. Desikan R, Clarke A, Hancock JT, Neill SJ. H2O2 activates a MAP kinase-like enzyme in Arabidopsis thaliana suspension cultures. Journal of Experimental Botany. 1999;50:1863-1866
  80. 80. Desikan R, Mackerness SAH, Hancock JT, Neill SJ. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiology. 2001;127:159-172
  81. 81. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science. 2002;7:405-410
  82. 82. Wolin, MS. and Mohazzab-H, KM. Mediation of signal transduction by oxidants. In: Scandalios, JG. (Ed.) Oxidative Stress and the Molecular Biology of Antioxidant Defenses. New York, Cold Spring Harbor Laboratory Press. pp. 21-48
  83. 83. 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 Journal. 2000;22:87-95
  84. 84. Bowler C, Van Montagu M, Inzé D. Superoxide dismutase and stress tolerance. Annual Review of Plant Physiology and Plant Molecular Biology. 1992;43:83-116
  85. 85. De Paula M, Pérez-Otaola M, Darder M, Torres M, Frutos G, Martinez-Honduvilla CJ. Function of the ascorbate–glutathione cycle in aged sunflower seeds. Physiologia Plantarum. 1996;96:543-550
  86. 86. De Tullio MC, Arrigoni O. The ascorbic acid system in seeds: To protect and to serve. Seed Science Research. 2003;13:249-260
  87. 87. Tommasi F, Paciolla C, de Pinto MC, De Gara L. A comparative study of glutathione and ascorbate metabolism during germination of Pinus pinea L. seeds. Journal of Experimental Botany. 2001;52:1647-1654
  88. 88. Eshdat Y, Holland D, Faltin Z, Ben-Hayyim G. Plant glutathione peroxidases. Physiologia Plantarum. 1997;100:234-240
  89. 89. Aalen RB. Peroxiredoxin antioxidants in seed physiology. Seed Science Research. 1999;9:285-295
  90. 90. Buitink J, Hoekstra FA, Leprince O. Biochemistry and biophysics of tolerance systems. In: Black M, Pritchard HW, editors. Desiccation and Survival in Plants: Drying without Dying. Wallingford: CABI Publishing; 2002. p. 293-318
  91. 91. Hara M, Terashima S, Fukaya T, Kuboi T. Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta. 2003;217:290-298
  92. 92. Fath A, Bethke P, Beligni V, Jones R. Active oxygen and cell death in cereal aleurone cells. Journal of Experimental Botany. 2002;53:1273-1282
  93. 93. Andarwulan N, Fardiaz D, Wattimena GA, Shetty K. Antioxidant activity associated with lipid and phenolic mobilization during seed germination of Pangium edule Reinw. Journal of Agricultural and Food Chemistry. 1999;47:3158-3163
  94. 94. De Gara L, de Pinto MC, Moliterni VMC, D’Egidio MG. Redox regulation and storage processes during maturation in kernels of Triticum durum. Journal of Experimental Botany. 2003;54:249-258
  95. 95. Otegui MS, Capp R, Staehelin LA. Developing seeds of Arabidopsis store different minerals in two types of vacuoles and in the endoplasmic reticulum. Plant Cell. 2002;14:1311-1327
  96. 96. Kato N, Esaka M. Changes in ascorbate oxidase gene expression and ascorbate levels in cell division and cell elongation in tobacco cells. Physiologia Plantarum. 1999;105:321-329
  97. 97. Papadakis AK, Siminis CI, Roubelakis-Angelakis KA. Reduced activity of antioxidant machinery is correlated with suppression of totipotency in plant protoplasts. Plant Physiology. 2001;126:434-444
  98. 98. Whitaker C, Beckett RP, Minibayeva FV, Kranner I. Alleviation of dormancy by reactive oxygen species in Bidens pilosa L. seeds. South African Journal of Botany. 2010;76:601-605
  99. 99. 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 Physiology. 2001;125:1591-1602 [PMC free article] [PubMed]
  100. 100. Asthir B, Duffus CM, Smith RC, Spoor W. Diamine oxidase is involved in H2O2 production in the chalazal cells during barley grain filling. Journal of Experimental Botany. 2002;53:677-682
  101. 101. Chen Y-H, Chao Y-Y, Hsu YY, Kao CH. Heme oxygenase is involved in H2O2-induced lateral root formation in apocynin-treated rice. Plant Cell Reports. 2013;32:219-226
  102. 102. Barba-Espin G, Diaz-Vivancos P, Clemente-Moreno MJ. Interaction between hydrogen peroxide and plant hormones during germination and the early growth of pea seedlings. Plant, Cell and Environment. 2010;33:981-994
  103. 103. Barba-Espín G, Diaz-Vivancos P, Job D, Belghazi M, Job C, Hernández JA. Understanding the role of H2O2 during pea seed germination: A combined proteomic and hormone profiling approach. Plant, Cell & Environment. 2011;34(11):1907-1919
  104. 104. Wang M, Heimovaara-Dijkstra S, Van Duijn B. Modulation of germination of embryos isolated from dormant and nondormant grains by manipulation of endogenous abscisic acid. Planta. 1995;195:586-592
  105. 105. Roach T, Beckett RP, Minibayeva FV. Extracellular superoxide production, viability and redox poise in response to desiccation in recalcitrant Castanea sativa seeds. Plant, Cell and Environment. 2010;33:59-75
  106. 106. 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]
  107. 107. 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

Written By

Fadime Eryılmaz Pehlivan

Submitted: March 20th, 2017 Reviewed: September 5th, 2017 Published: December 6th, 2017