Abstract
Reactive nitrogen species (RNS) are universal compounds that are constantly present in plant cells. RNS function depends on their actual level (the “nitrosative door” concept), duration of plant exposure to RNS and the context of the exposure. RNS are involved in the nitration of nucleic acids and fatty acids, posttranslational protein modifications (nitration and S-nitrosylation), and modulation of reactive oxygen species metabolism. RNS are regulatory molecules of various physiological processes in plants, including seed formation, maturation, dormancy and germination. The free radical theory of aging, well documented for animals, indicated that RNS participate in the regulation of the life span. Some data point to RNS contribution in preservation of seed vigor and/or regulation of seed longevity. Seed aging is a problem for biologists and agriculture, which could be solved by application of RNS, as a factor that may potentially expand seed vitality resulting in increased germination rate. The review is focused on RNS, particularly nitric oxide contribution to regulation of seed aging.
Introduction
Climate change causes weather extremes that influence plant mortality therefore, impacts biodiversity. Seed quality has an important bearing on the fate of the whole plant, and its development and lifespan. Seeds are the basis of plant production, the ultimate source of all food for humans and animals. The quality of seeds strongly influences the growth of the mature plants and determines their survival under environmental stress conditions.
The typical length of time that a seed survives (lifespan) varies among plant species. Seed longevity describes the length of time that seeds can remain viable and is an important factor for seedbanks in soil, seeds stored in warehouses, and the industries of seed production and sale (Walters et al., 2010; ). Moreover, seed lifespan is imprinted in the genes and influences efforts to preserve gene diversity in seedbanks (Walters et al., 2010).
Seed longevity depends on internal and external factors (). First of all, it is governed by the ability of seeds to withstand desiccation during maturation. Recalcitrant-type seeds are intolerant of water loss and are the most sensitive to aging, which is a major problem in their storage. Orthodox-type seeds are able to withstand low water content and are characterized by decreased metabolic activity. During long-term storage, seed longevity is determined by internal moisture content, external humidity, temperature, and oxygen pressure (Walters et al., 2010; ). Inappropriate storage conditions reduce seeds’ viability, and/or ability to germinate. Therefore, seed aging is associated with a reduction in longevity, mostly due to disturbances in metabolism and accumulation of harmful metabolites. Commonly, seed aging is associated with a loss of membrane integrity, modifications of nucleic acids, DNA degradation, impairment of protein and RNA synthesis, decreased energy metabolism ( and citation therein; ). Furthermore, uncontrolled reactive oxygen species (ROS) generation, and inefficient antioxidant machinery are involved in the loss of seed vigor and viability () (Figure 1A).
Figure 1
Seed aging is rather a slow process in the majority of plant species. Thus, artificial seed deterioration, including controlled deterioration treatment (CDT) or accelerated aging, are frequently applied in laboratory practice using established protocols (; ). Both treatments are based on application of sub-optimal conditions: elevated temperature and high humidity. The difference between CDT and accelerated aging is that during CDT seeds are imbibed to a precise water content prior to the warm temperature treatment (). Such treatments are commonly performed to accelerate aging and produce uniformly aged seeds that are easy to examine and compare in scientific research. However, specific conditions of CDT cause some differences between artificially and naturally aged seeds. The present review addresses the role of reactive nitrogen species (RNS) in the regulation of aging in seeds, mostly in the context of CDT application.
A Brief Introduction into Nitric Oxide (NO) Cellular Sources and Biosynthesis in Plants
For a long time, NO was recognized mainly as a pollutant of anthropogenic origin. Thereafter, it was discovered to be important in many physiological processes. NO was hailed as the “Molecule of the Year” by the journal Science in 1992. Experiments to discover NO biochemistry and its mode of action in living organisms were intensified after the 1998 Nobel Prize in Physiology and Medicine awarded for work on NO as a signaling molecule in the cardiovascular system. It was demonstrated that NO is emitted by plants, a discovery that launched 40 years of intensive research. The fine scheme of the milestone publications related to NO study in plants was done by and .
NO, and compounds that are formed from the interaction of NO with oxygen or superoxide anion (O2•−) known as reactive nitrogen species (RNS), are generated in almost every cellular compartment ( and citation therein).
Biochemistry of NO is linked to the formation of its different redox forms: nitrosonium cation (NO+), nitric oxide (•NO), and nitroxyl anion (NO−). In aqueous solution O2•−, which belongs to ROS, rapidly reacts with NO and gives rise to peroxynitrite (ONOO−) and its protonated form—peroxinitrous acid (ONOOH) (Stamler et al., 1992 and citation therein; and citation therein). NO also reacts with transition metal ions and other free radicals, and therefore it functions as an important regulator of metabolic processes (Stamler et al., 1992 and citation therein).
NO is synthesized via enzymatic and non-enzymatic pathways, which can be assigned to oxidative and reductive pathways. The best characterized and most acceptable enzymatic pathway of NO biosynthesis is a reaction catalyzed by nitrate reductase (NR) (). A recent report points on the primary function of the NIA1 isoform of NR as an NO-producing enzyme in Arabidopsis (). Moreover, some other molybdenum cofactor (Moco) containing enzymes are proposed to be involved in NO synthesis or homeostasis (). An open question is whether higher plants possess an enzyme that is homologous to the mammalian NO synthase (NOS). The only known case of such an enzyme in the plant kingdom was found and extensively examined in a green alga, Ostreococcus tauri (). Although NOS-like activity (a reaction requiring all the cofactors and co-substrates of the mammalian NOS) has been measured in higher plants, no NOS homologues in genomes or transcriptomes of land plants were found in available databases (). Doubts about the presence of L-arginine and the oxygen-dependent enzyme responsible for NO formation (like in mammalian NOS) led to the proposal that the term “NOS-like” be renamed “nitric oxide generating (NOG)” ().
The main non-enzymatic source of NO, and other reactive molecules derived from NO, is nitrite. Under acidic conditions, nitrite is protonated to nitrous acid (HNO2), which undergoes decomposition into different nitrogen oxides (NOx), depending on the redox state of the local environment of the reaction (Yamasaki, 2000; ). The rate of NO release from nitrite is increased in the presence of a mild reductants (e.g., ascorbic acid) (Yamasaki, 2000).
In seeds, only a few pathways of NO generation are discussed. During germination, NO production is thought to start shortly after imbibition and to correlate with oxygen depletion (). Under low oxygen conditions, mitochondria are one of the main producers of NO in plant cells (); therefore, the mitochondrial electron transport chain could be a potential source of NO in seeds at early stages of germination. The non-enzymatic reduction of nitrite to NO has been demonstrated in the apoplast of the aleurone layers of germinating barley (Hordeum vulgare L.) caryopsis ().
The lowered oxygen concentration in germinating seeds promotes NO formation by NR. This pathway was confirmed in sorghum (Sorghum bicolor L.) and tomato (Solanum lycopersicum L.) seeds (; ).
Another putative mechanism of NO synthesis in oxygen-limiting conditions is a reaction catalyzed by xanthine oxidoreductase (). During the first stages of germination, due to limited oxygen access, the oxidative routes of NO biosynthesis (hydroxylamine oxidation, NOS-like pathway) are unlikely. However, after the radical protrusion these pathways can be prevailing.
NO—A Crucial Regulator of Seed Germination and Plant Senescence
NO plays a beneficial role as the universal regulatory molecule in plant physiology. In seed biology, its function is concentration-dependent and can be described by the model of the “nitrosative door” (), which is comparable to the concept of “oxidative window for germination” associated with critical range of ROS level (). Many previous studies have indicated the importance of NO in the regulation of seed dormancy and the transition from a dormant to non-dormant state (; ; ). The NO mode of action and its cross-talk with plant hormones in seeds have also been previously summarized (; ; ). Therefore, there is no doubt that NO is the modulator of seed germination, and the positive effect of this molecule on dormancy breakage has been observed. NO and its donors were used to break seed dormancy, or accelerate germination and improve the vigor of developing seedlings (; ). Exogenous NO is also used in seed stratification treatment () to promote dormancy alleviation and enable faster germination.
At the molecular level, RNS are responsible for S-nitrosylation, tyrosine and tryptophan nitration of proteins, as well as nitration of fatty acids and nucleic acids (; ; ). Although such changes may constitute an integral signal transduction mechanism, in excess they cause degenerative processes linked to senescence, accelerated aging, or even cell death.
Evidence was provided that NO could be involved in the regulation of plant senescence. Treatment of soybean (Glycine max L.) cotyledons with NO deferred their aging via (among other effects) the stabilization of photosynthetic pigments (). In leaves, RNS contribute to the senescence process via interaction with ROS (). Low level of NO caused by the expression of bacterial NO dioxygenase (NOD, the enzyme that converts NO into nitrate in the presence of oxygen) in Arabidopsis led to a senescence-like phenotype (). Fumigation of NOD-type plants with NO reduced the senescence phenotype, indicating that RNS delay senescence in leaves. There are no NODs in plants, nevertheless, the action of this enzyme is comparable to the hemoglobins’ (Hbs) (). Plants nonsymbiotic Hbs (nHbs) decrease NO concentration (; ). There is a high probability that dioxygenase reaction of the system involving nHbs may also regulate plant senescence.
RNS in Seed Aging
An imbalance in cellular homeostasis and the time-dependent persistent alterations in the structure and function of biomolecules lead to the accumulation of cellular damages. These changes are universal features of aging in all living organisms, and they have been observed in aged seeds. Seed deterioration is a progressive, irreversible decrease in seed longevity accompanied by alterations of the nucleic acid structure (DNA fragmentation, chromosomal aberration, telomere length change, DNA methylation), lower capacity of the antioxidant system, and loss of membrane integrity. Deterioration process is also linked to the protein inactivation due to a variety of mechanisms, including non-enzymatic glycation through Amadori–Maillard reactions, oxidation of sulfhydryl groups, conversion of amino acids within the protein leading to partial folding or unfolding, dissociation to monomers or subunits, and condensation to polymers (; ; ).
The loss of seed vigor is manifested in a reduced germination rate, reduced number of seedlings, and increased number of abnormal seedlings. In laboratory conditions acceleration of seed aging is obtained through application of different aging treatments e.g. CDT. CDT was used in studies focused on establishing the role of RNS in the maintenance of seed quality. investigated NO action in the regulation of aging in elm (Ulmus pumila L.) seeds induced by CDT (37°C and 100% relative humidity). CDT decreased the vigor of seeds to 50% after 2 days, but application of sodium nitroprusside (SNP) before CDT supported high vigor (Figure 1B). Furthermore, the treatment of elm seeds with SNP before CDT significantly increased their germination rate. A burst of NO was observed at the beginning of the CDT aging of seeds, and the endogenous NO content decreased as CDT progressed ().
Similar data were reported for apple (Malus domestica Borkh.) embryos isolated from warm stratified seeds (subjected to accelerated aging). The maximum level of NO emissions occurred after 21 days of the treatment and was followed by the decline of NO emissions to the 70th day (). In general, apple seeds require a long period (3 months) of cold stratification for dormancy alleviation. Apple embryos that germinated after seeds were aged by warm stratification formed fewer seedlings, which also had developmental malformations (). It was previously demonstrated that developmental abnormalities can be reversed after NO fumigation ().
Oxidative damages due to the excessive formation of ROS are widely accepted to be the major contributors to seeds deterioration leading to their aging (; ). Detoxification mechanisms, including antioxidant metabolites and enzymes responsible for modulation of the ROS content, limit oxidative damages to proteins, lipids, and nucleic acids. Therefore, NO plays a role in the regulation of aging in seeds by counteracting ROS generation and stimulating the antioxidant system (Figures 1B, C). ROS have many deleterious effects on mitochondrial membranes, resulting in the release of cytochrome c into the cytosol to activate apoptotic cell death during the loss of seed viability (reviewed by ). Mitochondrial DNA is susceptible to ROS-induced damages, which lead to dysfunction of the organelles and are considered to be a major component of seed aging.
described the accumulation of H2O2 in mitochondria in artificially aged oat (Avena sativa L.) seeds that exhibited low vigor. The application of SNP to aged oat seeds had a protective effect, improving seed vigor and increasing ROS scavenging ability in mitochondria (Figure 1C). Higher activities of catalase, glutathione reductase, monodehydroascorbate reductase, and dehydroascorbate reductase in the ascorbate–glutathione (AsA–GSH) antioxidant system were also noticed. The activity of mitochondrial complex IV in the aged oat seeds decreased, but after application of NO, the activity increased to the level found in a non-aged caryopsis (). This was a striking finding, because NO is considered an inhibitor of cytochrome c oxidase. suggested that alternative oxidase was stimulated by NO, which may partly explain the decline in ROS production. In addition, protein abundance levels of some tricarboxylic acid cycle (TCA) enzymes, succinyl-CoA ligase and fumarate hydratase, in mitochondria from aged oat seeds increased after SNP treatment (Figure 1C). Thus, it was proposed that the NO treatment of aged seeds, could increase the capacity of some reactions of the TCA cycle and also the AsA–GSH cycle, leading to a lowering of the mitochondrial H2O2 content (). GSH is a marker of seed vigor, and a low GSH/GSSG ratio is linked to seed aging and loss of vigor () (Figure 1A). SNP pre-treatment of elm seeds subjected to CDT induced the expression of genes that encoded enzymes of the glutathione biosynthetic pathway and led to an increased level of GSH, which can protect seeds from oxidative damages resulting from ROS over-accumulation ().
The vigor of aged seeds depends on ethylene emission and seeds’ sensitivity to this hormone (). The physiological state and germination potential of seeds are linked to ethylene-NO cross-talk, ethylene biosynthesis, and signaling (). The interaction of NO and ethylene during dormancy release in apple embryos was demonstrated (). Embryos sensitivity to this hormone (regarded as a beneficial germination factor) increased after short-time fumigation with NO. In the context of seed aging, it was shown that pre-treatment of elm seeds (before CDT) with NO donors (SNP, GSNO) prevented a drastic decrease of expression in genes encoding ethylene biosynthesis enzymes: S-adenosyl-L-methionine (SAM) synthetase and 1-aminocyclopropane-1-carboxylic acid (ACC) synthase (ACS) () (Figure 1B). Taking into account that, on one hand, ethylene promoted germination of Arabidopsis seeds subjected to salinity stress (which induced oxidative stress), but on the other hand, SNP upregulated ACS2 expression, resulting in a lower H2O2 level (), it appears that the NO-ethylene synergistic interaction delays seed aging caused by oxidative stress.
In contrast, high ethylene emission typically occurs during senescence of leaves or petals and during fruit ripening (). ACC in the presence of NO can be converted via non-enzymatic reaction to ethylene (). This raises the question whether an over-accumulation of RNS and ROS could stimulate non-enzymatic ethylene emission during seed aging (even during dormancy), which may accelerate deterioration.
SAM is the metabolite that links biosynthesis of NO, ethylene, and polyamines (PAs) (; ). PAs are regulators of plant growth and development that also modulate seed aging. Their content generally decreases during seed aging (), and they are known to maintain vigor and viability during accelerated aging (Yalamalle et al., 2019). A reduction in the PAs level seems to be a significant prelude to senescence signals (). In contrast, germination of apple embryos induced by NO fumigation was associated with increased activity of polyamine oxidase (PAO) (). Conversion of spermine by PAO results in liberation of H2O2, the key molecule for seed dormancy breakage. Thus, NO-stimulated catabolism of PAs in seed aging is unwelcome, while NO-dependent H2O2 formation due to an enhancement of PAO activity may be beneficial during seed germination. However, prolonged NO action could be potentially destructive because it stimulates the generation of harmful ROS. So again, whether NO plays a positive or negative role in seed biology, including acceleration of aging, is concentration- and time-dependent.
Seed germination, vigor, and aging were linked to ABA control (). In dormant apple embryos, NO fumigation reduced sensitivity to ABA () as well as expression of the transcription factor abscisic acid insensitive 5 (ABI5) (). used seeds of two lines of Chinese kale (Brassica oleracea L.) with different ABA content to show that a low endogenous ABA level increased sensitivity of seeds to artificial aging. In ABA-deficient or insensitive Arabidopsis mutants, reduction of seed longevity was clearly associated with a lack of dormancy ().
NO participates in post-translational protein modifications (PTMs), including S-nitrosylation of proteins, which was suggested to play a beneficial role in seed germination. In Arabidopsis seeds, S-nitrosylation of ABI5 promoted germination by stimulating ABI5 protein degradation (). Furthermore, markedly decreased levels of SNO-proteins during prolonged seed aging can be recognized as a signal for selective protein degradation, similar to that observed for ABI5 (). Protein S-nitrosylation is a reversible PTM that was shown to enhance the activities of antioxidant enzymes, thereby reducing cellular ROS levels. Therefore, S-nitrosylation can indirectly protect against uncontrolled protein carbonylation (an irreversible PTM occurring as a reaction to oxidative stress) (). It was demonstrated in recalcitrant Antiaris toxicaria Lesch. seeds, that pre-treatment with NO stimulated germination by causing S-nitrosylation of antioxidant enzymes, which modified their activities ().
In elm seeds, S-nitrosylated proteins were accumulated at an early stage of aging (). The study of showed that S-nitrosylation in elm seeds affected proteins of carbohydrate metabolism that participate in glycolysis, the mitochondrial TCA cycle, and pentose phosphate pathways. The authors concluded that S-nitrosylation, and therefore NO signaling, can be one of the mechanisms involved in regulation of deterioration process in seeds.
Conclusions
Aging leads to a decrease in the quality of seeds (Figure 1A), which limits not only agricultural production but also the preservation of global biodiversity. Studies aiming to understand the mechanisms underlying seed aging and the associated decrease in seed quality employ the artificial accelerated aging approaches that allow to obtain a pool of equally aged seeds. Treatments that effectively protect seeds against aging or prevent seed deterioration require further evaluation.
NO and other compounds belonging to the RNS family appear to mitigate the negative effects of seed aging. Treatment of seeds with NO or NO donors before induction of aging, or at the initial stages of aging (Figures 1B, C), activates the antioxidant system, which delays or prevents the initiation of mechanisms that induce aging. The application of NO donors at some stages of the aging process activates defence mechanisms (e.g., reversible redox PTMs, AsA–GSH cycle), which lead to an improvement in seed quality (Figure 1C), even if the aging process was activated earlier. Although evidence has been provided that NO can partially prevent seed deterioration caused by aging, its application in the seed industry requires further research.
Funding
This work was performed during realization of the project financed by National Science Centre, Poland 2016/23/B/NZ9/03462 given to UK.
Statements
Author contributions
Conceptualization: UK, KC, PS, AG. Writing—original draft preparation: UK, KC, AG. Writing—editing and figure preparation: PS, JZ, AW. Supervision: AG. Funding acquisition: UK. All authors contributed to the article and approved the submitted version.
Acknowledgments
The authors are sorry to all the colleagues whose papers were not cited in this mini-review due to space limitation.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
1
AlbertosP.Romero-PuertasM. C.TatematsuK.MateosI.Sánchez-VicenteI.NambareE.et al. (2015). S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nat. Commun.6, 8669. doi: 10.1038/ncomms9669
2
Andryka-DudekP.CiackaK.WiśniewskaA.BogatekR.GniazdowskaA. (2019). Nitric oxide-induced dormancy removal of apple embryos is linked to alterations in expression of genes encoding ABA and JA biosynthetic or transduction pathways and RNA nitration. Int. J. Mol. Sci.20, 1007. doi: 10.3390/ijms20051007
3
Arasimowicz-JelonekM.Floryszak-WieczorekJ. (2019). A physiological perspective on targets of nitration in NO-based signaling networks in plants. J. Exp. Bot.70, 4379–4389. doi: 10.1093/jxb/erz300
4
ArcE.GallandM.GodinB.CueffG.RajjouL. (2013a). Nitric oxide implication in the control of seed dormancy and germination. Front. Plant Sci.4, 346. doi: 10.3389/fpls.2013.00346
5
ArcE.SechetJ.CorbineauF.RajjouL.Marion-PollA. (2013b). ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Front. Plant Sci.4, 63. doi: 10.3389/fpls.2013.00063
6
BaiX.YangL.TianM.ChenJ.ShiJ.YangY.et al. (2011). Nitric oxide enhances desiccation tolerance of recalcitrant antiaris toxicaria seeds via protein S-nitrosylation and carbonylation. PloS One6, e20714. doi: 10.1371/journal.pone.0020714
7
BaillyC.El-Maarouf-BouteauH.CorbineauF. (2008). From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. C. R. Biol.331, 806–814. doi: 10.1016/j.crvi.2008.07.022
8
BenderD.SchwarzG. (2018). Nitrite-dependent nitric oxide synthesis by molybdenum enzymes. FEBS Lett.592, 2126–2139. doi: 10.1002/1873-3468.13089
9
BethkeP. C. (2004). Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell16, 332–341. doi: 10.1105/tpc.017822
10
BykovaN. V.HuJ.MaZ.IgamberdievA. U. (2015). “The role of reactive oxygen and nitrogen species in bioenergetics, metabolism, and signaling during seed germination,” in Reactive oxygen and nitrogen species signaling and communication in plants. signaling and communication in plants. Eds. GuptaK. J.IgamberdievA. U. (Cham: Springer), 177–195.
11
ChenD.ShaoQ.YinL.YounisA.ZhengB. (2019). Polyamine function in plants: Metabolism, regulation on development, and roles in abiotic stress responses. Front. Plant Sci.9, 1945. doi: 10.3389/fpls.2018.01945
12
CorbineauF. (2012). Markers of seed quality: from present to future. Seed. Sci. Res.22, S61–S68. doi: 10.1017/S0960258511000419
13
CorpasF. J.Begara-MoralesJ. C.Sánchez-CalvoB.ChakiM.BarrosoJ. B. (2015). “Nitration and S-nitrosylation: Two post-translational modifications (PTMs) mediated by reactive nitrogen species (RNS) and their role in signalling processes of plant cells,” in Reactive oxygen and nitrogen species signaling and communication in plants, signaling and communication in plants, 23rd edn. Eds. GuptaK. J.IgamberdievA. U. (Cham: Springer), 267–281.
14
DębskaK.KrasuskaU.BudnickaK.BogatekR.GniazdowskaA. (2013). Dormancy removal of apple seeds by cold stratification is associated with fluctuation in H2O2, NO production and protein carbonylation level. J. Plant Physiol.170, 480–488. doi: 10.1016/j.jplph.2012.11.018
15
Del CastelloF.NejamkinA.CassiaR.Correa-AragundeN.FernándezR.ForesiN.et al. (2019). The era of nitric oxide in plant biology: Twenty years tying up loose ends. Nitric. Oxide85, 17–27. doi: 10.1016/J.NIOX.2019.01.013
16
DurzanD. J.PedrosoM. C. (2002). Nitric oxide and reactive nitrogen oxide species in plants. Biotechnol. Genet. Eng. Rev.19, 293–338. doi: 10.1080/02648725.2002.10648032
17
El-Maarouf-BouteauH.MazuyC.CorbineauF.BaillyC. (2011). DNA alteration and programmed cell death during ageing of sunflower seed. J. Exp. Bot.62, 5003–5011. doi: 10.1093/jxb/err198
18
ForesiN.Correa-AragundeN.ParisiG.CaloG.SalernoG.LamattinaL. (2010). Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell22, 3816–3830. doi: 10.1105/tpc.109.073510
19
FuY.-B.AhmedZ.DiederichsenA. (2015). Towards a better monitoring of seed ageing under ex situ seed conservation. Conserv. Physiol.3, cov026. doi: 10.1093/conphys/cov026
20
GardnerP. R.GardnerA. M.MartinL. A.SalzmanA. L. (1998). Nitric oxide dioxygenase: An enzymic function for flavohemoglobin. Proc. Natl. Acad. Sci.95, 10378–10383. doi: 10.1073/pnas.95.18.10378
21
GniazdowskaA.DobrzyńskaU.BabańczykT.BogatekR. (2007). Breaking the apple embryo dormancy by nitric oxide involves the stimulation of ethylene production. Planta225, 1051–1057. doi: 10.1007/s00425-006-0384-z
22
GniazdowskaA.KrasuskaU.CzajkowskaK.BogatekR. (2010). Nitric oxide, hydrogen cyanide and ethylene are required in the control of germination and undisturbed development of young apple seedlings. Plant Growth Regul.61, 75–84. doi: 10.1007/s10725-010-9452-2
23
GodberB. L. J.DoelJ. J.SapkotaG. P.BlakeD. R.StevensC. R.EisenthalR.et al. (2000). Reduction of nitrite to nitric oxide catalyzed by xanthine oxidoreductase. J. Biol. Chem.275, 7757–7763. doi: 10.1074/jbc.275.11.7757
24
GuptaK. J.IgamberdievA. U.ManjunathaG.SeguS.MoranJ. F.NeelawarneB.et al. (2011). The emerging roles of nitric oxide (NO) in plant mitochondria. Plant Sci.181, 520–526. doi: 10.1016/j.plantsci.2011.03.018
25
HancockJ. T.NeillS. J. (2019). Nitric oxide: Its generation and interactions with other reactive signaling compounds. Plants8, 41. doi: 10.3390/plants8020041
26
HeH.De Souza VidigalD.Basten SnoekL.SchnabelS.NijveenH.HilhorstH.et al. (2014). Interaction between parental environment and genotype affects plant and seed performance in Arabidopsis. J. Exp. Bot.65, 6603–6615. doi: 10.1093/jxb/eru378
27
HeY.XueH.LiY.WangX. (2018). Nitric oxide alleviates cell death through protein S-nitrosylation and transcriptional regulation during the ageing of elm seeds. J. Exp. Bot.69, 5141–5155. doi: 10.1093/jxb/ery270
28
HuD.MaG.WangQ.YaoJ.WangY.PritchardH. W.et al. (2012). Spatial and temporal nature of reactive oxygen species production and programmed cell death in elm (Ulmus pumila L.) seeds during controlled deterioration. Plant Cell Environ.35, 2045–2059. doi: 10.1111/j.1365-3040.2012.02535.x
29
HungK. T.KaoC. H. (2003). Nitric oxide counteracts the senescence of rice leaves induced by abscisic acid. J. Plant Physiol.160, 871–879. doi: 10.1078/0176-1617-01118
30
IgamberdievA. U.BykovaN. V.HillR. D. (2011). Structural and functional properties of class 1 plant hemoglobins. IUBMB Life63, 146–152. doi: 10.1002/iub.439
31
JasidS.GalatroA.VillordoJ. J.PuntaruloS.SimontacchiM. (2009). Role of nitric oxide in soybean cotyledon senescence. Plant Sci.176, 662–668. doi: 10.1016/j.plantsci.2009.02.007
32
KolbertZ.BarrosoJ. B.BrouquisseR.CorpasF. J.GuptaK. J.LindermayrC.et al. (2019). A forty year journey: The generation and roles of NO in plants. Nitric. Oxide93, 53–70. doi: 10.1016/j.niox.2019.09.006
33
KrannerI.BirtićS.AndersonK. M.PritchardH. W. (2006). Glutathione half-cell reduction potential: a universal stress marker and modulator of programmed cell death? Free Radic. Biol. Med.40, 2155–2165. doi: 10.1016/j.freeradbiomed.2006.02.013
34
KrasuskaU.CiackaK.BogatekR.GniazdowskaA. (2014). Polyamines and nitric oxide link in regulation of dormancy removal and germination of apple (Malus domestica Borkh.) embryos. J. Plant Growth Regul.33, 590–601. doi: 10.1007/s00344-013-9408-7
35
KrasuskaU.CiackaK.Andryka-DudekP.BogatekR.GniazdowskaA. (2015a). “Nitrosative Door” in seed dormancy alleviation and germination,” in Reactive oxygen and nitrogen species signaling and communication in plants, Signaling and communication in plants, 1st edn., vol. 23 . Eds. GuptaK. J.IgamberdievA. U. (Cham: Springer), 215–237.
36
KrasuskaU.DębskaK.OtulakK.BogatekR.GniazdowskaA. (2015b). Switch from heterotrophy to autotrophy of apple cotyledons depends on NO signal. Planta242, 1221–1236. doi: 10.1007/s00425-015-2361-x
37
KrasuskaU.CiackaK.OrzechowskiS.FettkeJ.BogatekR.GniazdowskaA. (2016). Modification of the endogenous NO level influences apple embryos dormancy by alterations of nitrated and biotinylated protein patterns. Planta244, 877–891. doi: 10.1007/s00425-016-2553-z
38
KurekK.Plitta-MichalakB.RatajczakE. (2019). Reactive oxygen species as potential drivers of the seed aging process. Plants8, 174. doi: 10.3390/plants8060174
39
LaraT. S.LiraJ. M. S.RodriguesA. C.RakocevicM.AlvarengaA. A. (2014). Potassium nitrate priming affects the activity of nitrate reductase and antioxidant enzymes in tomato germination. J. Agric. Sci.6, 72–80. doi: 10.5539/jas.v6n2p72
40
LiZ.PengJ.WenX.GuoH. (2013). Ethylene-insensitive3 is a senescence-associated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell25, 3311–3328. doi: 10.1105/tpc.113.113340
41
LinY.YangL.PaulM.ZuY.TangZ. (2013). Ethylene promotes germination of Arabidopsis seed under salinity by decreasing reactive oxygen species: Evidence for the involvement of nitric oxide simulated by sodium nitroprusside. Plant Physiol. Biochem.73, 211–218. doi: 10.1016/j.plaphy.2013.10.003
42
LiuJ.XueT.ShenY. (2019). Effect of nitric oxide on seed germination and dormancy in empress trees in horttechnology. Horttechnology29, 271–275. doi: 10.21273/HORTTECH04250-18
43
MaoC.ZhuY.ChengH.YanH.ZhaoL.TangJ.et al. (2018). Nitric oxide regulates seedling growth and mitochondrial responses in aged oat seeds. Int. J. Mol. Sci.19, 1052. doi: 10.3390/ijms19041052
44
Mata-PérezC.Sánchez-CalvoB.PadillaM. N.Begara-MoralesJ. C.ValderramaR.CorpasF. J.et al. (2017). Nitro-fatty acids in plant signaling: New key mediators of nitric oxide metabolism. Redox Biol.11, 554–561. doi: 10.1016/j.redox.2017.01.002
45
MatillaA. J. (1996). Polyamines and seed germination. Seed. Sci. Res.6, 81–93. doi: 10.1017/S096025850000310X
46
MishinaT. E.LambC.ZeierJ. (2007). Expression of a nitric oxide degrading enzyme induces a senescence programme in Arabidopsis. Plant Cell Environ.30, 39–52. doi: 10.1111/j.1365-3040.2006.01604.x
47
MohnM.ThaqiB.Fischer-SchraderK. (2019). Isoform-specific NO synthesis by Arabidopsis thaliana nitrate reductase. Plants8, 67. doi: 10.3390/plants8030067
48
PerazzolliM.DominiciP.Romero-PuertasM. C.ZagoE.ZeierJ.SonodaM.et al. (2004). Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. Plant Cell16, 2785–2794. doi: 10.1105/tpc.104.025379
49
RatajczakE.MałeckaA.CiereszkoI.StaszakA. (2019). Mitochondria are important determinants of the aging of seeds. Int. J. Mol. Sci.20, 1568. doi: 10.3390/ijms20071568
50
RochaB. S.GagoB.PereiraC.BarbosaR. M.BartesaghiS. O.LundbergJ.et al. (2011). Dietary nitrite in nitric oxide biology: a redox interplay with implications for pathophysiology and therapeutics. Curr. Drug Targets12, 1351–1363. doi: 10.2174/138945011796150334
51
SanoN.RajjouL.NorthH. M.DebeaujonI.Marion-PollA.SeoM. (2016). Staying alive: molecular aspects of seed longevity. Plant Cell Physiol.57, 660–674. doi: 10.1093/pcp/pcv186
52
SanzL.AlbertosP.MateosI.Sánchez-VicenteL.LechónI.Fernández-MarcosM.et al. (2015). Nitric oxide (NO) and phytohormones crosstalk during early plant development. J. Exp. Bot.66, 2857–2868. doi: 10.1093/jxb/erv213
53
SchausbergerC.RoachT.StögglW.ArcE.Finch-SavageW. E.KrannerI. (2019). Abscisic acid-determined seed vigour differences do not influence redox regulation during ageing. Biochem. J.476, 965–974. doi: 10.1042/BCJ20180903
54
ShamsM.YildirimE.AgarG.ErcisliS.EkinciM.DursulL.et al. (2018). Nitric oxide alleviates copper toxicity in germinating seed and seedling growth of Lactuca sativa L. Not. Bot. Hort. Agrobot. Cluj-Napoca46, 167–172. doi: 10.15835/nbha46110912
55
SimontacchiM.JasidS.PuntaruloS. (2004). Nitric oxide generation during early germination of sorghum seeds. Plant Sci.167, 839–847. doi: 10.1016/j.plantsci.2004.05.028
56
SiriwitayawanG.DownieA. B.GeneveR. L. (2003). Ethylene evolution is positively correlated with seed vigor in sweet corn and tomato seed lots with differing vigor levels but similar germination capacity. J. Am. Soc. Hortic. Sci.128, 608–614. doi: 10.21273/jashs.128.4.0608
57
ŠírováJ.SedlářováM.PiterkováJ.LuhováA.PetřivalskýY. (2011). The role of nitric oxide in the germination of plant seeds and pollen. Plant Sci.181, 560–572. doi: 10.1016/j.plantsci.2011.03.014
58
StamlerJ.SingelD.LoscalzoJ. (1992). Biochemistry of nitric oxide and its redox-activated forms. Science (80- )258, 1898–1902. doi: 10.1126/science.1281928
59
WaltersC.BallesterosD.VertucciV. A. (2010). Structural mechanics of seed deterioration: Standing the test of time. Plant Sci.179, 565–573. doi: 10.1016/j.plantsci.2010.06.016
60
XinX.LinX. H.ZhouY. C.ChenX. L.LiuX.LuX. X. (2011). Proteome analysis of maize seeds: The effect of artificial ageing. Physiol. Plant143, 126–138. doi: 10.1111/j.1399-3054.2011.01497.x
61
YalamalleV. R.TomarB. S.JainS. K.AroraA.KumarA.MunshiA. D. (2019). Spermine induced protection of onion seed vigour and viability during accelerated ageing. J. Environ. Biol.40, 1079–1083. doi: 10.22438/jeb/40/5/MRN-1047
62
YamasakiH. (2000). Nitrite-dependent nitric oxide production pathway: implications for involvement of active nitrogen species in photoinhibition in vivo. Philos. Trans. R. Soc. B. Biol. Sci.355, 1477–1488. doi: 10.1098/rstb.2000.0708
Summary
Keywords
germination, nitric oxide, seed viability, aging, vigor
Citation
Ciacka K, Krasuska U, Staszek P, Wal A, Zak J and Gniazdowska A (2020) Effect of Nitrogen Reactive Compounds on Aging in Seed. Front. Plant Sci. 11:1011. doi: 10.3389/fpls.2020.01011
Received
07 February 2020
Accepted
19 June 2020
Published
08 July 2020
Volume
11 - 2020
Edited by
Marek Petrivalsky, Palacký University, Olomouc, Czechia
Reviewed by
Natalia V. Bykova, Agriculture and Agri-Food Canada (AAFC), Canada; Petr Smýkal, Palacký University, Olomouc, Czechia
Updates
Copyright
© 2020 Ciacka, Krasuska, Staszek, Wal, Zak and Gniazdowska.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Urszula Krasuska, urszula_krasuska@sggw.edu.pl
This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science
†ORCID: Katarzyna Ciacka orcid.org/0000-0003-1485-2901; Urszula Krasuska orcid.org/0000-0001-8373-4509; Pawel Staszek orcid.org/0000-0001-8532-5151; Agnieszka Gniazdowska orcid.org/0000-0003-0077-3743
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.