Abstract
The investigation aimed at determining the effect of nitric oxide on antioxidant defense system of spring maize (Zea mays L.) genotypes namely, LM 11 (stress susceptible) and CML 32 (stress tolerant), that showed differential tolerance towards heat stress. Seed priming with a NO donor, sodium nitroprusside (SNP) improved seedling growth and induced varied defense mechanisms, under stress conditions. 75 μM SNP improved seedling lengths and their biomasses. It specifically enhanced catalase (CAT) activity in the roots of stressed seedlings of the two genotypes. However, it could induce CAT activity only in LM 11 shoots, under heat stress. It also enhanced peroxidase (POX) activity in CML 32 roots. However, such induction of POX activity with SNP treatment was not observed in LM 11 roots. This showed that NO increased the H2O2 scavenging efficiency of CML 32 genotype by enhancing the cumulative activation of CAT and POX in its roots. However, it did not induce activation of any of the H2O2 detoxifying enzymes in CML 32 shoots which showed that ascorbate–glutathione cycle remained non-operational in shoots of SNP-treated seedlings of the tolerant genotype, under high temperature stress. With seed priming, superoxide dismutase (SOD) activity increased in both the tissues of LM 11 seedlings. The shoots of SNP primed CML 32 seedlings, however, did not show any effect on SOD activity which illustrated that nitric oxide might act as a direct scavenger of superoxide radicals in CML 32 seedlings. SNP decreased the contents of H2O2 and MDA and increased proline content in seedlings of both the genotypes indicating reduced oxidative damage. The results thus showed that nitric oxide might induce different mechanisms of stress tolerance in these maize genotypes.
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Alavi SMN, Arvin MJ, Kalantari KM (2014) Salicylic acid and nitric oxide alleviate osmotic stress in wheat (Triticum aestivum L.) seedlings. J Plant Interact 9:683–688
Arasimowicz M, Floryszak-Wieczorak J (2007) Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Sci 172:876–887
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207
Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273
Boogar AR, Salehi H, Jowkar A (2014) Exogenous nitric oxide alleviates oxidative damage in turfgrasses under drought stress. South Afr J Bot 92:78–82
Bowler C, Montagu MV, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Phys 43:83–116
Cechin I, Cardoso GS, Fumis T, Corniani N (2015) Nitric oxide reduces oxidative damage induced by water stress in sunflower plants. Bragantia Campinas 74:200–216
Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Methods Enzymol 2:764–775
Dash S, Mohanty N (2002) Response of seedlings to heat-stress in cultivars of wheat: growth temperature-dependent differential modulation of photosystem I and II activity and foliar antioxidant defense capacity. J Plant Physiol 159:49–59
Davey MW, Stals E, Pains B, Keulemans J, Swennen RL (2005) High through put determination of malondialdehyde in plant tissues. Anal Biochem 347:201
Ding HD, Zhang XH, Liu H, Liang JS, Liu B (2012) Involvement of calcium and calmodulin signalling in adaptation to heat stress induced oxidative stress in Solanum lycopersicum L. leaves. Afr J Biotechnol 11:3259–3269
El-Beltagi HS, Ahmed OK, Hegazy AE (2016) Protective effect of nitric oxide on high temperature induced oxidative stress in wheat (Triticum aestivum) callus culture. Not Sci Biol 8:192–198
Enyisi SI, Umoh VJ, Whong CMZ, Abdullahi IO, Alabi O (2014) Chemical and nutritional value of maize products obtained from selected markets. Afr J Food Sci Technol 5:100–104
Esterbaur H, Grill D (1978) Seasonal variation of glutathione and glutathione reductase in seedlings of Picea abies. Plant Physiol 61:119–121
Fan H, Du C (2012) Effect of nitric oxide on proline metabolism in cucumber seedlings under salinity stress. J Am Soc Sci 137:127–133
Farooq MH, Bramley J, Palta A, Siddique KHM (2011) Heat stress in wheat during reproductive and grain filling phases. Crit Rev Plant Sci 30:491–507
Fotopoulos V, Antoniou C, Filippou P, Mylona P, Fasoula D, Ioannides I, Polidoros A (2014) Application of sodium nitroprusside results in distinct antioxidant gene expression patterns in leaves of mature and senescing Medicago truncatula plants. Protoplasma 251:973–978
Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide and glutathione-associated mechanisms of acclamatory stress tolerance and signaling. Plant Physiol 100:241–254
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Gosavi GU, Jadhav AS, Kale AA, Gadakh SR, Pawar BD, Chimote VP (2014) Effect of heat stress on proline, chlorophyll content, heat shock proteins and antioxidant enzyme activity in sorghum (Sorghum bicolor) at seedling stage. Indian J Biotechnol 13:356–363
Gould K, Lamotte O, Klinguer A, Pugin A, Wendehenne D (2003) Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ 26:1851–1862
Groß F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and pro-oxidants in plant defence responses. Front Plant Sci 4:1–15
Hasanuzzaman M, Nahar K, Alam MM, Futija M (2012) Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum L.) seedlings by modulating the antioxidant defense and glyoxalase system. Aust J Crop Sci 6:1314–1323
Hasanuzzaman M, Nahar K, Mahabub A, Roychowdhury R, Futija M (2013) Physiological, biochemical and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684
Heath RL, Packer L (1968) Photo peroxidation in isolated chloroplasts. Arch Biochem Biophys 125:189–198
Ismail GSM (2012) Protective role of nitric oxide against arsenic-induced damages in germinating mung bean seeds. Acta Physiol Plant 34:1303–1311
James D, Tarafdar A, Biswas K, Sathyavathi TC, Padaria JC, Kumar PA (2015) Development and characterization of a high temperature stress responsive subtractive cDNA library in Pearl Millet (Pennisetum glaucum L.). Indian J Exp Biol 53:543
Kausar F, Shahbaz M, Ashraf M (2013) Protective role of foliar-applied nitric oxide in Triticum aestivum under saline stress. Turk J Bot 37:1155–1165
Khan MIR, Iqbal N, Masood A, Per TS, Khan NA (2013) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal Behav 8:26374
Lamattina L, Garcia-Mata C, Graziano M, Pagnusat G (2003) Nitric oxide the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136
Liu S, Dong YJ, Xu LL, Kong J, Bai XY (2013) Roles of exogenous nitric oxide in regulating equilibrium and moderating oxidative stress in cotton seedlings during salt stress. J Plant Sci Plant Nutr 34:929–941
Lowry OH, Rosebrough NJ, Frase AT, Randall RJ (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–275
Marklund S, Marklund G (1974) Involvement of superoxide anion radical in the auto-oxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:169–174
Miller G, Suzuki N, Ciftci- Yilmaz S, Mittler R (2010) Reactive oxygen homeostatis and signalling during drought and salinity stress. J Agric Res 45:269–276
Nakano Y, Asada K (1987) Purification of ascorbate peroxidase in spinach chloroplast: its inactivation in ascorbate depleted medium and reactivation by monodehyroascorbate radical. Plant Cell Physiol 28:131–140
Naveed S, Aslam M, Maqbool MA, Bano S, Zaman QU, Ahmad RM (2014) Physiology of high temperature stress tolerance at reproductive stages in maize. J Anim Plant Sci 24:1141–1145
Nejadalimoradi H, Nasibi F, Manoochehri K, Zanganeh R (2014) Effect of seed priming with l-arginine and sodium nitroprusside on some physiological parameters and antioxidant enzymes of sunflower plants exposed to salt stress. Agric Commun 2:23–30
Ostrovskaya LK, Truch VV, Mikhailik OM (2009) Superoxide dismutase activation in response to lime-induced chlorosis. New Phytol 114:39–45
Oz MT, Eyidogan F, Yucel M, Oktem HA (2015) Functional role of nitric oxide under abiotic stress conditions. In: Khan MN, Mobin M, Mohammad F, Corpas FJ (eds) Nitric oxide action in abiotic stress responses in plants. Springer International Publishing, Switzerland, pp 21–41
Parankusam S, Adimulam SS, Mathur PB, Sharma KK (2017) Nitric oxide (NO) in plant heat stress tolerance: current knowledge and perspectives. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01582
Ranum P, Pena-Rosas JP, Garcia-Casal MN (2014) Global maize production, utilization and consumption. Ann Acad Sci 1312:105–112
Sadeghipour O (2016) Pretreatment with nitric oxide reduces lead toxicity in cowpea (Vigna unguiculata L.). Arch Biol Sci 68:165–175
Sairam RK, Deshmukh PS, Saxena DC (1998) Role of antioxidant systems in wheat genotypes tolerance to water stress. Biol Plant 41:387–394
Sanchez-Casas P, Klessig DF (1994) A salicylic acid binding activity and a salicylic acid-inhibitable catalase activity are present in a variety of plant species. Plant Physiol 106:1675–1779
Shannon LM, Kay E, Law JY (1966) Peroxidase isozymes from horse radish roots. I. Isolation and physical properties. J Biol Chem 241:2166–2172
Singh PH, Kaur S, Daizy R, Batish VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:289–297
Singh NB, Yadav K, Amist N (2014) Positive effects of nitric oxide on Solanum lycopersicum. J Plant Interact 9:10–18
Sinha AK (1971) Calorimetric assay of catalase. Anal Biochem 47:389–394
Song L, Ding W, Zhao M, Sun B, Zhang L (2006) Nitric oxide protects against oxidative stress under heat stress in calluses from two genotypes of reed. Plant Sci 171:449–458
Tewari AK, Tripathy BC (1999) Assimilation of chlorophyll biosynthetic reactions to temperature stress in cucumber (Cucumis sativus L.). Planta 208:431–437
Wang C, Zhang SH, Li W, Wang PF, Li L (2011) Nitric oxide supplementation alleviates ammonium toxicity in the submerged macrophyte Hydrilla verticillata (L.) Royle. Ecotoxicol Environ Safe 74:67–73
Yali H, Bingru H (2010) Differential responses to heat stress in activities and isozymes of four antioxidant enzymes for two cultivars of Kentucky bluegrass contrasting in heat tolerance. J Ami Soc Hortic Sci 135:116–124
Yildiztugay E, Ozfidan-Konakci C, Kucukoduk M (2014) Exogenous nitric oxide (as sodium nitroprusside) ameliorates polythene glycol-induced osmotic stress in hydroponically grown maize roots. J Plant Growth Regul 33:683–696
Zhou B, Guo Z, Xing J, Huang B (2005) Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis. J Exp Bot 56:3223–3228
Acknowledgements
We are grateful to Dr. Gurjit Kaur Gill, Sr. Maize Breeder, Department of Plant Breeding and Genetics, Punjab Agricultural University, Ludhiana, for providing maize genotypes for this investigation.
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Kaur, K., Kaur, K. Nitric oxide improves thermotolerance in spring maize by inducing varied genotypic defense mechanisms. Acta Physiol Plant 40, 55 (2018). https://doi.org/10.1007/s11738-018-2632-9
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DOI: https://doi.org/10.1007/s11738-018-2632-9