Abstract
NO has an important role in the control of plant development, growth, and the response to abiotic stress. In our recent paper it was demonstrated that NO affected the salt-induced changes in free amino acid levels in maize.1 Since polyamines are synthesized from lysine and arginine, it was supposed that their concentrations are also influenced by NO. Cadaverine levels were increased by a NO donor and decreased by an inhibitor of NO synthesis in salt-stressed maize. These findings indicate that NO participates in the mediation of the effect of salt on cadaverine content. The coordinated changes in the NO and cadaverine levels may be involved in regulating of the response to salt stress in maize.
Keywords: cadaverine, free amino acids, lysine, nitric oxide, maize, polyamines, salt stress
Salt stress results in severe damage to crops and consequently in yield losses. High salt concentrations lead to the reprogramming of the metabolism. The accumulation of protective metabolites may reduce the salt-induced damage to plant tissues. Stress-induced changes in polyamine levels are especially important, since these compounds are involved in many physiological processes, namely in the control of growth, development, and the response of plants to various stresses.2-4 The relationship detected between changes in the level of stress-induced injuries and the polyamine content either after exogenous application or in transgenic plants with modified polyamine metabolism, revealed the protective role of polyamines during abiotic stresses. Changes in polyamine levels often derive from the altered expression of the corresponding genes, as shown in the case of putrescine in salt-stressed grapes, where the increased expression of the gene encoding arginine decarboxylase was observed.5 While the role of putrescine, spermine, and spermidine in the reduction of stress-induced damage has been investigated in many plant species, the involvement of cadaverine in the stress response has not been intensively studied.2-4 Cadaverine also participates in the control of growth and development under both optimal and stress conditions (reviewed in 6). Based on the scavenging of free radicals in the common ice plant the protective role of cadaverine against salt-induced injuries was attributed to its antioxidative function.7 This role could be very important in reducing of the salt-induced damage since reactive oxygen species accumulate to toxic concentrations in stressed plants.8 In addition, the exogenous application of cadaverine improved the growth of Brassica juncea under salt stress due to its effect on photosynthetic pigments, nitrate reductase activity, organic nitrogen, and soluble proteins.9
An important effect of polyamines is the induction of NO formation, as observed in Arabidopsis.10-12 NO is involved in the regulation of plant growth and development under both optimal and stress conditions.13,14 The protective role of NO during salt stress was demonstrated after exogenous application, which reduced the damage in rice, lupine, and cucumber (reviewed in ref. 14). NO affected the balance between the carbon and nitrogen metabolisms, activated antioxidants, and modified membrane permeability to various ions.
In our recent study it was shown that the pharmacological modification of NO levels affected the growth of maize under salt stress conditons.1 (Z)-1-[N-(2-aminoethyl)-N-(2-ammonioethyl)amino]diazen-1-ium-1,2-diolate (DETA/NO), a NO donor, reduced the salt-induced loss in fresh weight, while nitro-l-arginine (L-NNA), an inhibitor of NO synthesis, increased it. Similarly to other stresses, NaCl also induced oxidative stress, as indicated by increases in the glutathione disulphide content and in the reduction potential of the glutathione/glutathione disulphide couple. NO reduced this effect of salt stress on the glutathione redox state. Based on the simultaneous changes in the redox state of glutathione and in the concentration of several amino acids, it was hypothesized that the effect of salt stress on the amino acid metabolism is mediated by redox signaling and that NO is involved in this process. The comparison of the effect of salt on the proline content with and without the simultaneous pharmacological modification of the NO level showed that NO induced a great increase in the proline concentration during the recovery phase. This may contribute to the improvement of salt tolerance in maize. NO induced proline accumulation not only in maize but also Medicago truncatula via the increased expression and activity of pyrroline-5-carboxylate synthase, a key enzyme of proline synthesis.15
The amino acid and polyamine metabolisms are interconnected, so it was assumed that NO may also influence polyamine levels. Indeed, NO was shown to increase the putrescine concentration under optimal growth conditions in Medicago truncatula due to the induction of arginine decarboxylase at both gene expression and enzyme activity levels.15 In the present experiments the addition of DETA/NO to the nutrient solution with or without NaCl increased cadaverine levels compared with plants treated only with NaCl for 3 d (Fig. 1). These changes coincided with a decrease in the lysine content after 3 d of DETA/NO or DETA/NO+NaCl treatment (Table 1). Thus, the increase in the cadaverine content was the result of its greater synthesis from lysine after these treatments. However, after 3 d of treatment with KNO2 (which was used as a control to distinguish effects observed strictly as the result of NO from those caused by the decomposition of NO to nitrate or nitrite), the elevated cadaverine concentration was not accompanied by a corresponding decrease in the lysine content. In addition, after 11 d of treatment and at the end of the 7-d recovery period, there was no relationship between changes in lysine and cadaverine contents. Thus, at these sampling points the cadaverine content may also be influenced by its degradation. Although the other polyamines, putrescine, spermidine, and spermine, were not present at detectable levels at all sampling points, it can be suggested that NO may have a negative effect on their levels, since higher concentrations of these polyamines were detected after the inhibition of NO synthesis by L-NNA (data not shown).
Figure 1. Effect of NO on salt-induced changes in the concentration of cadaverine. Cadaverine content was measured in the youngest fully developed leaves after 0, 3, or 11 d of treatment with various compounds or after 7 d of recovery (R7d, without these compounds). NaCl: 150 mM; DETA/NO (NO donor): 5 μM; DETA: 5 μM; L-NNA (inhibitor of NO synthesis): 1 mM; KNO2 (control for decomposition of NO): 150 mM. Values indicated by different letters are significantly different at the P < 0.005 level. The significant difference is 2.4.
Table 1. Effect of NO on salt-induced changes in the relative concentration of lysine.
| 3 d treatment | 11 d treatment | 7d recovery | |
|---|---|---|---|
| NaCl | 128a | 77b | 153c |
| DETA/NO | 79b | 184d | 66b |
| DETA/NO + NaCl | 59e | 84b | 378f |
| DETA | 140a | 129a | 14g |
| DETA + NaCl | 151c | 56e | 210d |
| L-NNA | 109a | 245h | 112a |
| L-NNA + NaCl | 102a | 72b | 131a |
| KNO2 | 115a | 65a | 35e |
Lysine concentrations were measured in the youngest fully developed leaves. The relative concentrations were calculated as the percentage of the values measured before the treatment and after 3 or 11 d of treatment or 7 d of recovery. NaCl: 150 mM; DETA/NO (NO donor): 5 μM; DETA: 5 μM; L-NNA (inhibitor of NO synthesis): 1 mM; KNO2 (control for decomposition of NO): 150 mM. Values indicated by different letters are significantly different at the P < 0.005 level. The significant difference is 18.
In conclusion, the present findings indicate that salt-induced changes in cadaverine levels are modified by NO. Cadaverine may be involved in the signaling pathways activated during salt stress, as described in heat-stressed common ice plants.16 In these pathways, various hormones and secondary messengers may also participate, in addition to NO, as suggested for putrescine, spermidine, and spermine (reviewed in 4). In addition, cadaverine could be a source of H2O2 through its degradation by amine oxidases,17 as described in soybean hypocotyls.18 H2O2 is involved in redox signaling pathways which activate various protective mechanisms. Besides having an indirect role in the stress response, increased cadaverine levels or its exogenous addition may also improve salt tolerance directly due to its antioxidant function.7
Disclosure of Potential Conflicts of Interest
No potential conflicts of interest were disclosed.
Acknowledgments
This work was supported by the Hungarian Scientific Research Fund (OTKA K 83642, CNK 80781). The authors are grateful for the help of Krisztina Szirtes (Budapest Technical and Economic University, Hungary).
Glossary
Abbreviations:
- DETA/NO
(Z)-1-[N-(2-aminoethyl)-N-(2-ammonioethyl)amino]diazen-1-ium-1,2-diolate
- L-NNA
nitro-L-arginine
References
- 1.Boldizsár A, Simon-Sarkadi L, Szirtes K, Soltész A, Szalai G, Keyster M, Ludidi N, Galiba G, Kocsy G. Nitric oxide affects salt-induced changes in free amino acid levels in maize. J Plant Physiol. 2013;170:1020–7. doi: 10.1016/j.jplph.2013.02.006. [DOI] [PubMed] [Google Scholar]
- 2.Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF. Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta. 2010;231:1237–49. doi: 10.1007/s00425-010-1130-0. [DOI] [PubMed] [Google Scholar]
- 3.Gill SS, Tuteja N. Polyamines and abiotic stress tolerance in plants. Plant Signal Behav. 2010;5:26–33. doi: 10.4161/psb.5.1.10291. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Bitrián M, Zarza X, Altabella T, Tiburcio AF, Alcázar R. Polyamines under abiotic stress: metabolic crossroads and hormonal crosstalks in plants. Metabolites. 2012;2:516–28. doi: 10.3390/metabo2030516. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Liu JH, Nakajima I, Moriguchi T. Effects of salt and osmotic stresses on free polyamine content and expression of polyamine biosynthetic genes in Vitis vinifera. Biol Plant. 2011;55:340–4. doi: 10.1007/s10535-011-0050-6. [DOI] [Google Scholar]
- 6.Tomar PC, Lakra N, Mishra SN. Cadaverine – a lysine catabolite involved in plant growth and development. Plant Signal Behav. 2013;8(10):e25850. doi: 10.4161/psb.25850. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Kuznetsov V, Shorina M, Aronova E, Stetsenko L, Rakitin V, Shevyakova N. NaCl- and ethylene-dependent cadaverine accumulation and its possible protective role in the adaptation of the common ice plant to salt stress. Plant Sci. 2007;172:363–70. doi: 10.1016/j.plantsci.2006.09.012. [DOI] [Google Scholar]
- 8.Szalai G, Kellős T, Galiba G, Kocsy G. Glutathione as an antioxidant and regulatory molecule in plants subjected to abiotic stresses. J Plant Growth Regul. 2009;28:66–80. doi: 10.1007/s00344-008-9075-2. [DOI] [Google Scholar]
- 9.Tomar PC, Lakra N, Mishra SN. Effect of cadaverine on Brassica juncea (L.) under multiple stress. Indian J Exp Biol. 2013;51:758–63. [PubMed] [Google Scholar]
- 10.Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EI, Scherer GF. Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol. 2006;47:346–54. doi: 10.1093/pcp/pci252. [DOI] [PubMed] [Google Scholar]
- 11.Yamasaki H, Cohen MF. NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants? Trends Plant Sci. 2006;11:522–4. doi: 10.1016/j.tplants.2006.09.009. [DOI] [PubMed] [Google Scholar]
- 12.Wimalasekera R, Tebartz F, Scherer GF. Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci. 2011;181:593–603. doi: 10.1016/j.plantsci.2011.04.002. [DOI] [PubMed] [Google Scholar]
- 13.Kocsy G, Tari I, Vanková R, Zechmann B, Gulyás Z, Poór P, Galiba G. Redox control of plant growth and development. Plant Sci. 2013;211:77–91. doi: 10.1016/j.plantsci.2013.07.004. [DOI] [PubMed] [Google Scholar]
- 14.Siddiqui MH, Al-Whaibi MH, Basalah MO. Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma. 2011;248:447–55. doi: 10.1007/s00709-010-0206-9. [DOI] [PubMed] [Google Scholar]
- 15.Filippou P, Antoniou C, Fotopoulos V. The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. Free Radic Biol Med. 2013;56:172–83. doi: 10.1016/j.freeradbiomed.2012.09.037. [DOI] [PubMed] [Google Scholar]
- 16.Kuznetsov VV, Rakitin VY, Sadomov NG, Dam DV, Stetsenko LA, Shevyakova NI. Do polyamines participate in the long-distance translocation of stress signals in plants? Russ J Plant Physiol. 2002;49:120–30. doi: 10.1023/A:1013776631284. [DOI] [Google Scholar]
- 17.Cona A, Rea G, Angelini R, Federico R, Tavladoraki P. Functions of amine oxidases in plant development and defence. Trends Plant Sci. 2006;11:80–8. doi: 10.1016/j.tplants.2005.12.009. [DOI] [PubMed] [Google Scholar]
- 18.Campestre MP, Bordenave CD, Origone AC, Menéndez AB, Ruiz OA, Rodríguez AA, Maiale SJ. Polyamine catabolism is involved in response to salt stress in soybean hypocotyls. J Plant Physiol. 2011;168:1234–40. doi: 10.1016/j.jplph.2011.01.007. [DOI] [PubMed] [Google Scholar]