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Seed Priming with Sodium Nitroprusside and H2O2 Confers Better Yield in Wheat Under Salinity: Water Relations, Antioxidative Defense Mechanism and Ion Homeostasis

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Abstract

To mitigate the deleterious effects of abiotic stresses signaling molecules play a significant role. The present study was aimed to assess the responses of two differentially salt-tolerant wheat genotypes (Fsd-2008 and S-24) to exogenously applied sodium nitroprusside (SNP) (donor of nitric oxide), hydrogen peroxide (H2O2) as well as their combined application as seed priming under saline stress. Before sowing seeds were primed with each treatment as soaking for 16 h. Salinity markedly decreased the growth, nutrient uptake and yield, while enhanced the H2O2, malondialdehyde, osmolytes accumulation, antioxidative defense mechanism and Na+ uptake in both wheat cultivars. Comparatively less increase in Na+ uptake was recorded in genotype S-24 in comparison with genotype Fsd-2008. Seed priming with H2O2 and SNP improved the growth and yield, in association with increment in leaf photosynthetic pigments, water relations as well as accumulation of osmolytes. The content of non-enzymatic antioxidant components as well as activities of antioxidant enzymes were also further increased by the seed priming with signaling molecules in both wheat genotypes. Improvement in K+/Na+ ratio due to seed priming was also found in both wheat genotypes but more improvement was in genotype S-24. In conclusion, SNP and H2O2 applied salt tolerance was associated with improved photosynthetic pigments, water relations, osmolytes accumulation, antioxidative defense mechanism, and improved Na+ discrimination.

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References

  • Ahmad P, Abdel-Latef AA, Hashem A, Abd-Allah EF, Gucel S, Tran LSP (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:1–11

    Google Scholar 

  • Akram MS, Ashraf M, Shahbaz M, Akram NA (2009) Growth and photosynthesis of salt-stressed sunflower (Helianthus annuus) plants as affected by foliar-applied different potassium salts. J Pant Nutr Soil Sci 172:884–893

    Google Scholar 

  • Alam DS (2001) Wheat-An important edible crop of Pakistan. Pak Econ 51

  • Alencar NL, Gadelha CG, Gallao IM, Dolder AHM, Prisco JT, Gomes-Filho E (2015) Ultrastructural and biochemical changes induced by salt stress in Jatropha curcas seeds during germination and seedling development. Funct Plant Biol 42:865–874

    CAS  PubMed  Google Scholar 

  • Ali Q, Ashraf M (2011) Exogenously applied glycinebetaine enhances seed and seed oil quality of maize (Zea mays L.) under water deficit conditions. Environ Exp Bot 71:249–259

    CAS  Google Scholar 

  • Ali Q, Daud MK, Haider MZ, Ali S, Rizwan M, Aslam N, Noman A, Iqbal N, Shahzad F, Deeba F, Ali I, Zhu SJ (2017) Seed priming by sodium nitroprusside improves salt tolerance in wheat (Triticum aestivum L.) by enhancing physiological and biochemical parameters. Plant Physiol Biochem 119:50–58

    CAS  PubMed  Google Scholar 

  • Ali Q, Javed MT, Noman A, Haider MZ, Waseem M, Iqbal N, Waseem M, Shah MS, Shahzad F, Perveen R (2018) Assessment of drought tolerance in mung bean cultivars/lines as depicted by the activities of germination enzymes, seedling’s antioxidative potential and nutrient acquisition. Arch Agron Soil Sci 64(1):84–102

  • Arnon DI (1949) Copper enzyme in isolated chloroplasts polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

  • Ashfaque F, Khan MIR, Khan NA (2014) Exogenously applied H2O2 promotes proline accumulation, water relations, photosynthetic efficiency and growth of wheat (Triticum aestivum L.) under salt stress. Ann Res Rev Biol 4:105–120

    Google Scholar 

  • Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93

    CAS  PubMed  Google Scholar 

  • Ashraf M, Ali Q (2008) Relative membrane permeability and activities of some antioxidant enzymes as the key determinants of salt tolerance in canola (Brassica napus L.). Environ Exp Bot 63(1–3):266–273

    CAS  Google Scholar 

  • Ashraf MA, Ashraf M (2012) Salt-induced variation in some potential physiological attribute of two genetically diverse spring wheat (Triticum aestivum L.) cultivars: photosynthesis and photosystem II efficiency. Pak J Bot 44:53–64

    CAS  Google Scholar 

  • Ashraf M, Harris P (2009) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 16:3–16

    Google Scholar 

  • Ashraf MA, Rasheed R, Hussain I, Iqbal M, Haider MZ, Parveen S, Sajid MA (2014) Hydrogen peroxide modulates antioxidant system and nutrient relation in maize (Zea mays L.) under water-deficit conditions. Arch Agron Soil Sci 61:507–523

    Google Scholar 

  • Assaha DVM, Ueda A, Saneoka H, Al-Yahyai R, Yaish MW (2017) The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Front Physiol 8:509. https://doi.org/10.3389/fphys.2017.00509

    Article  PubMed  PubMed Central  Google Scholar 

  • Azevedo Neto AD, Prisco JT, Eneas-Filho J, Medeiros JV, Gomes-Filho E (2005) Hydrogen peroxide pre-treatment induces salt-stress acclimation in maize plants. J Plant Physiol 162:1114–1122

    PubMed  Google Scholar 

  • Bai XJ, Liu LJ, Zhang CH, Ge Y, Cheng WD (2011) Effect of H2O2 pretreatment on Cd tolerance of different rice cultivars. Rice Sci 18:29–35

    Google Scholar 

  • Banu MNA, Hoque MA, Watanable-Sugimoto M, Matsoka K, Nakamura Y, Murata SY, Y, (2009) Proline and glycinebetaine induce antioxidant defense gene expression and suppress cell death in cultured tobacco cells under salt stress. J Plant Physiol 166:146–156

    CAS  PubMed  Google Scholar 

  • Barba-Espin G, Diaz-Vivancos P, Job D, Belghazi M, Job C, Hernandez JA (2011) Understanding the role of H2O2 during pea seed germination: a combined proteomic and hormone profiling approach. Plant Cell Environ 34:1907–1919

    CAS  PubMed  Google Scholar 

  • Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    CAS  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analyt Biochem 72(1–2):248–254

    CAS  PubMed  Google Scholar 

  • Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468

    CAS  Google Scholar 

  • Chance M, Maehly AC (1955) Assay of catalases and peroxidases. Method Enzymol 2:764–817

    Google Scholar 

  • Chen J, Xiang L, Chao W, Yin SS, Li XL, Hu WJ et al (2015) Nitric oxide ameliorates zinc oxide nanoparticles-induced phytotoxicity in rice seedlings. J Hazard Mater 297:173–182

    CAS  PubMed  Google Scholar 

  • Chung JS, Zhu J, Bressan RA, Hasegawa PM, Shi H (2008) Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J 53:554–565

    CAS  PubMed  Google Scholar 

  • Dar MI, Naikoo MI, Rehman F, Naushin F, Khan FA (2016) Proline accumulation in plants: roles in stress tolerance and plant development. In: Iqbal N (ed) Osmolytes and plants acclimation to changing environment: emerging omics technologies. Springer, India, pp 155–165

    Google Scholar 

  • Davis J, Freitas F (1970) Physical and chemical methods of soil and water analysis, soil bulletin 10. Rome, Food and Agricultural Organizations

    Google Scholar 

  • Dietz KJ, Mittler R, Noctor G (2016) Recent progress in understanding the role of reactive oxygen species in plant cell signaling. Plant Physiol 171:1535–1539

    CAS  PubMed  PubMed Central  Google Scholar 

  • Egbichi KM, Ludidi N (2014) Effect of exogenous application of nitric oxide on salt stress responses of soybean. South Afr J Bot 90:131–136

    CAS  Google Scholar 

  • Fan H, Guo S, Jiao Y, Zhang R, Li J (2007) Effects of exogenous nitric oxide on growth, active oxygen species metabolism, and photosynthetic characteristics in cucumber seedlings under NaCl stress. Front Agric China 1(3):308–314

    Google Scholar 

  • Fan HF, Du CX, Guo SR (2012) Effect of nitric oxide on proline metabolism in cucumber seedlings. Plant Soil 318:37–45

    Google Scholar 

  • Fan HF, Du CX, Ding L, Xu YL (2013) Effects of nitric oxide on the germination of cucumber seeds and antioxidant enzymes under salinity stress. Acta Physiol Plant 35:2707–2719

    CAS  Google Scholar 

  • Gadjev I, Stone JM, Gechev TS (2008) Programmed cell death in plants: new insights into redox regulation and the role of hydrogen peroxide. Int Rev Cell Mol Biol 270:87–144

    CAS  PubMed  Google Scholar 

  • Gao Y, Guo YK, Lin SH, Fang YY, Bai JG (2010) Hydrogen peroxide pretreatment alters the activity of antioxidant enzymes and protects chloroplast ultrastructure in heat-stressed cucumber leaves. Scient Hort 126:20–26

    CAS  Google Scholar 

  • Ge XM, Cai HL, Lei X, Zou X, Yue M, He JM (2015) Heterotrimeric protein mediates ethylene-induced stomatal closure via hydrogen peroxide synthesis in Arabidopsis. Plant J 82:138–150

    CAS  PubMed  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases occurrence in higher plants. Plant Physiol 59:309–314

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gondim FA, Gomes-Filho E, Costa JH, Alencar NLM, Prisco JT (2012) Catalase plays a key role in salt stress acclimation induced by hydrogen peroxide pretreatment in maize. Plant Physiol Biochem 56:62–71

    CAS  PubMed  Google Scholar 

  • Gondim FA, Miranda RDS, Gomes-filho E, Prisco JT (2013) Enhanced salt tolerance in maize plants induced by H2O2 leaf spraying is associated with improved gas exchange rather than with non-enzymatic antioxidant system. Theor Exp Plant Physiol 25:251–260

    Google Scholar 

  • Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307

    CAS  Google Scholar 

  • Guo Y, Tian Z, Yan D, Zhang J, Qin P (2005) Effects of nitric oxide on salt stress tolerance in Kosteletzkya virginica. Life Sci J 6:67–75

    CAS  Google Scholar 

  • Habib N, Ashraf M (2014) Effect of exogenously applied nitric oxide on water relations and ionic composition of rice (Oryza sativa L.) plants under salt stress. Pak J Bot 46(1):111–116

    Google Scholar 

  • Habib N, Ashraf M, Ali Q, Perveen R (2012) Response of salt stressed okra (Abelmoschus esculentus Moench.) plants to foliar-applied glycine betaine and glycine betaine containing sugarbeet extract. South Afr J Bot 83:151–158

    CAS  Google Scholar 

  • Habib N, Ashraf M, Shahbaz M (2013) Effect of exogenously applied nitric oxide on some key physiological attributes of rice (Oryza sativa L.) plants under salt stress. Pak J Bot 45(5):1563–1569

    CAS  Google Scholar 

  • Habib N, Akram MS, Javed MT, Azeem M, Ali Q, Shaheen HL, Ashraf M (2016) Nitric oxide regulated improvement in growth and yield of rice plants grown under salinity: antioxidant defense system. Appl Ecol Environ Res 14(5):91–105

    Google Scholar 

  • Habib N, Ali Q, Ali S, Javed MT, Haider MZ, Perveen R, Shahid MR, Rizwan M, Abdel-Daim MM, Elkelish A, Bin-Jumah M (2020) Use of nitric oxide and hydrogen peroxide for better yield of wheat (Triticum aestivum L.) under water deficit conditions: growth, osmoregulation, and antioxidative defense mechanism. Plants 9:285

    CAS  PubMed Central  Google Scholar 

  • Hala EM, Alaa E, Rajendra AGM (2015) Role of hydrogen peroxide pretreatment on developing antioxidant capacity in the leaves of tomato plant (Lycopersicon esculentum) grown under saline stress. Int J Adv Res 3(2):878–879

    Google Scholar 

  • Hameed A, Iqbal N (2014) Chemo-priming with mannose, mannitol and H2O2 mitigate drought stress in wheat. Cereal Res Commun 42:450–462

    CAS  Google Scholar 

  • Hasanuzzaman M, Hossain MA, da-Silva JAT, Fujita M, (2012) Plant responses and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. Perspectives and strategies, Crop stress and its management, pp 261–315

    Google Scholar 

  • Hayat SSA, Hasan M, Mori M, Fariduddin Q, Ahmad A (2010) Nitric oxide: chemistry, biosynthesis, and physiological role. In: Hayat S, Mori M, Pichtel J, Ahmad A (eds) Nitric oxide in plant physiology. Wiley, Germany, pp 1–16

    Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7(11):1456–1466

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hernandez-Barrera A, Velarde-Buendia A, Zepeda I, Sanchez F, Quinto C, Sanchez-Lopez R et al (2015) Hyper, a hydrogen peroxide sensor, indicates the sensitivity of the Arabidopsis root elongation zone to aluminum treatment. Sensor 15:855–867

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hoque MA, Okuma E, Nakamara Y, Shimoishi Y, Murata Y (2008) Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification system and reduce NaCl-induced damage in cultured tobacco cells. J Plant Physiol 165:813–824

    CAS  PubMed  Google Scholar 

  • Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W, Li HY, Burritt DJ, Fujita M, Tran LS (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:1–19

    Google Scholar 

  • Huang AX, Wang YS, She XP, Mu J, Zhao JL (2015) Copper amineoxidase-catalysed hydrogen peroxide involves production of nitric oxide in darkness-induced stomatal closure in broad bean. Funct Plant Biol 42:1057–1067

    CAS  PubMed  Google Scholar 

  • Iakimova ET, Woltering EJ (2015) Nitric oxide prevents wound-induced browning and delays senescence through inhibition of hydrogen peroxide accumulation in fresh-cut lettuce. Innov Food Sci Emerg Technol 30:157–169

    CAS  Google Scholar 

  • Iqbal N, Umar S, Khan NA, Khan MIR (2014) A new perspective of phytohormones in salinity tolerance: regulation of proline metabolism. Environ Exp Bot 100:34–42

    CAS  Google Scholar 

  • Ishibashi Y, Yamamoto K, Tawaratusmida T, Yuasa T, Iwaya-Inoue M (2008) Hydrogen peroxide scavenging regulates germination ability during wheat (Triticum aestivum L.) seed maturation. Plant Signal Behav 3(3):183–188

    PubMed  PubMed Central  Google Scholar 

  • Ishibashi Y, Yamaguchi H, Yussa T, Iwaya-Inoue M, Arima S, Zheng SH (2011) Hydrogen peroxide spraying alleviates drought stress in soyabean plants. J Plant Physiol 168:1562–1567

    CAS  PubMed  Google Scholar 

  • Jamil S, Ali Q, Iqbal M, Javed MT, Iftikhar W, Shahzad F, Perveen R (2015) Modulations in plant water relations and tissue-specific osmoregulation by foliar-applied ascorbic acid and the induction of salt tolerance in maize plants. Braz J Bot 38(3):527–538

    Google Scholar 

  • Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. trends Plant Sci 20:586–594

  • Julkunen-Tiitto R (1985) Phenolic constituents in the leaves of northern willows: methods for the analysis of certain phenolics. J Agric Food Chem 33:213–217

  • Kanwal H, Ashraf M, Hamed M (2013) Water relations and ionic composition in the seedlings of some newly developed and candidate cultivars of wheat (Triticum aestivum L.) under saline conditions. Pak J Bot 45(4):1221–1227

    CAS  Google Scholar 

  • Kausar A, Ashraf MY, Niaz M (2014) Some physiological and genetic determinants of salt tolerance in sorghum (Sorghum Bicolor L.) Moench), biomass production and nitrogen metabolism. Pak J Bot 46(2):515–519

    Google Scholar 

  • Kaya C, Sonmez O, Aydemir S, Dikilitaş M (2013) Mitigation effects of glycinebetaine on oxidative stress and some key growth parameters of maize exposed to salt stress. Turk J Agric For 37:188–194

    CAS  Google Scholar 

  • Kirk JTO, Allen RL (1965) Dependence of chloroplast pigment synthesis on protein synthesis: effect of actidione. Biochem Biophys Res Commun 21:523–530

    CAS  PubMed  Google Scholar 

  • Kong X, Wang T, Li W, Tang W, Zhang D, Dong H (2016) Exogenous nitric oxide delays salt-induced leaf senescence in cotton (Gossypium hirsutum L.). Acta Physiol Plant 38:61

    Google Scholar 

  • Kumar RR, Sharma SK, Gadpayle KA, Singh K, Sivaranjani R, Goswami S, Rai RD (2012) Mechanism of action of hydrogen peroxide in wheat thermotolerance interaction between antioxidant isoenzymes, proline and cell membrane. Afr J Biotechnol 11:14368–14379

    CAS  Google Scholar 

  • Li JT, Qui ZB, Zhang XW, Wang LS (2011) Exogenous hydrogen peroxide can enhance tolerance of wheat seedlings to salt stress. Acta Physiol Plant 33:835–842

    CAS  Google Scholar 

  • Liao WB, Xiao HL, Zhang ML (2009) Role and relationship of nitric oxide and hydrogen peroxide in adventitious root development of marigold. Acta Physiol Plant 31:1279–1289

    CAS  Google Scholar 

  • Liao WB, Huang GB, Yu JH, Zhang ML, Shi XL (2011) Nitric oxide and hydrogen peroxide are involved in indole-3-butyric acid-induced adventitious root development in marigold. J Hortic Sci Biotech 86:159–165

    CAS  Google Scholar 

  • Liao WB, Zhang ML, Huang GB, Yu JH (2012) Ca2+ and Ca Mare involved in NO and H2O2-induced adventitious root development in marigold. J Plant Growth Regul 31:253–264

    CAS  Google Scholar 

  • Lin AH, Wang YQ, Tang JY, Xue P, Li CL, Liu LC et al (2012) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide induced: leaf cell death in rice. Plant Physiol 158:451–464

    CAS  PubMed  Google Scholar 

  • Liu WW, Chen HB, Lu XY, Rahman MJ, Zhou ZS, BY, (2015) Identification of nitric oxide responsive genes in the floral buds of Litchi chinensis. Biol Plant 59:115–122

    CAS  Google Scholar 

  • Mansour MMF, Ali EF (2017) Glycine betaine in saline conditions: an assessment of the current state of knowledge. Acta Physiol Plant 39–56

  • Mignolet-Spruyt L, Xu E, Idanheimo N, Hoeberichts FA, Muhlenbock P, Brosche M, Van-Breusegem F, Kangasjarvi J (2016) Spreading the news: subcellular and organellar reactive oxygen species production and signaling. J Exp Bot 67:3831–3844

    CAS  PubMed  Google Scholar 

  • Miller GAD, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33(4):453–467

    CAS  PubMed  Google Scholar 

  • Miranda RS, Gomes-Filho E, Prisco JT, Alvarez-Pizarro JC (2016) Ammonium improves tolerance to salinity stress in Sorghum bicolor plants. Plant Growth Regul 78:121–131

    CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K et al (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    CAS  PubMed  Google Scholar 

  • Moussa HR, Mohamed MAEFH (2011) Role of nitric acid or H2O2 in antioxidant defense system of Pisum sativum L. under drought stress. Nat Sci 9:211–216

    Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implication of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Plant Physiol 58:166–170

    CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Review Plant Biol 59:651–681

    CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Fujita M (2016) Roles of osmolytes in plant adaptation to drought and salinity. In: Nazar R, Khan N, Iqbal N (eds) Osmolytes and plants acclimation to changing environment: emerging omics technologies, Springer India, pp 37–68

    Google Scholar 

  • Nazir N, Ashraf M, Ejaz R (2001) Genomic relationships in oilseed Brassica with respect to salt tolerance-photosynthetic capacity and ion relations. Pak J Bot 33:483–501

    Google Scholar 

  • Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Riberio D, Wilson I (2008) Nitric oxide, stomatal closure and abiotic stress. J Exp Bot 59:165–176

    CAS  PubMed  Google Scholar 

  • Noreen S, Ashraf M (2008) Alleviation of adverse effects of salt stress on sunflower (Helianthus annuus L.) by exogenous application of salicylic acid: growth and photosynthesis. Pak J Bot 40(4):1657–1663

    CAS  Google Scholar 

  • Qian HF, Peng XF, Han X, Ren J, Zhan KY, Zhu M (2014) The stress factor, exogenous ascorbic acid, affects plant growth and the antioxidant system in Arabidopsis thaliana. Russ J Plant Physl 61:467–475

    CAS  Google Scholar 

  • Reddy PS, Jogeswar G, Rasineni GK, Maheswari M, Reddy AR, Varshney RK, Kishor PK (2015) Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench]. Plant Physiol Biochem 94:104–113

    PubMed  Google Scholar 

  • Rejeb BK, Abdelly C, Savoure A (2014) How reactive oxygen species and proline face stress together. Plant Physiol Biochem 80:278–284

    PubMed  Google Scholar 

  • Richards SL, Wilkins KA, Swarbreck SW, Anderson AA, Habib N, Smith AG, Mcainsh M, Davies JM (2015) The hydroxyl radical in plants: from seed to seed. J Exp Bot 66(1):37–46

    CAS  PubMed  Google Scholar 

  • Sairam RK, Srivastava GC, Agarwal S, Meena RC (2005) Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biol Plant 49:85–91

    CAS  Google Scholar 

  • Santisree P, Bhatnagar-Mathur P, Sharma KK (2015) NO to drought-multifunctional role of nitric oxide in plant drought. Plant Sci 239:44–55

    CAS  PubMed  Google Scholar 

  • Savvides A, Ali S, Tester M, Fotopoulos V (2015) Chemical priming of plants against multiple abiotic stresses. Trends Plant Sci 21:329–340

    PubMed  Google Scholar 

  • Shan C, Yan Z, Liu M (2015) Nitric oxide participates in the regulation of the ascorbate-glutathione cycle by exogenous jasmonic acid in the leaves of wheat seedlings under drought stress. Protoplasma 252:1397–1405

    CAS  PubMed  Google Scholar 

  • Sheokand S, Bhankar V, Sawhney V (2010) Ameliorative effect of exogenous nitric oxide on oxidative metabolism in NaCl treated chickpea plants. Braz J Plant Physiol 22:81–90

    Google Scholar 

  • Shi Q, Ding F, Wang X, Wei M (2007) Exogenous nitric oxide protects cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45:542–550

    CAS  PubMed  Google Scholar 

  • Shi K, Li X, Zhang H, Zhang G, Liu Y, Zhou Y et al (2015a) Guard cell hydrogen peroxide and nitric oxide mediate elevated CO2-induced stomatal movement in tomato. New Phytol 208:342–353

    CAS  PubMed  Google Scholar 

  • Shi Y, Liu J, Xin N, Gu R, Qin Zhu L, Zhang C et al (2015b) Signals induced by exogenous nitric oxide and their role in controlling brown rot disease caused by monilinia fructicola in postharvest peach fruit. J Genet Plant Pathol 81:68–76

    CAS  Google Scholar 

  • Singh HP, Batish DR, Kaur G, Arora K, Kohli RK (2008) Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot 63:158–167

    CAS  Google Scholar 

  • Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    CAS  PubMed  Google Scholar 

  • Tan J, Wang C, Xiang B, Han R, Guo Z (2013) Hydrogen peroxide and nitric oxide mediated cold and dehydration induced myo-inositol phosphate synthase that confers multiple resistances to abiotic stresses. Plant Cell Environ 36:288–299

    CAS  PubMed  Google Scholar 

  • Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60:795–804

    CAS  PubMed  Google Scholar 

  • Tanou G, Job C, Belghazi M, Molassiotis A, Diamantidis G, Job S (2010) Proteomic signatures uncover hydrogen peroxide and nitric oxide cross-talk signaling network in citrus plants. J Proteome Res 9:5994–6006

    CAS  PubMed  Google Scholar 

  • Tariq A, Masroor M, Khan A, Jaime A, da Teixeira S, Mohd I, Naeem M (2011) Role of salicylic acid in promoting salt stress tolerance and enhanced artemisinin production in Artemisia annua L. J Plant Growth Regul 30:425–435

    Google Scholar 

  • Terzi R, Kadioglu A, Kalaycioglu E, Saglam A (2014) Hydrogen peroxide pretreatment induces osmotic stress tolerance by influencing osmolyte and abscisic acid levels in maize leaves. J Plant Interact 9:559–565

    CAS  Google Scholar 

  • Ullah S, Kolo Z, Egbichi I, Keyster M, Ludidi N (2016) Nitric oxide influences glycine betaine content and ascorbate peroxidase activity in maize. South Afr J Bot 105:218–225

    CAS  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Protective role of exogenous ployamines. Plant Sci 151:59–66

    CAS  Google Scholar 

  • Verma S, Mishra SN (2005) Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. J Plant Physiol 162:669–677

    CAS  PubMed  Google Scholar 

  • Wahid A, Perveen M, Gelani S, Basra SMA (2007) Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. J Plant Physiol 164:283–294

    CAS  PubMed  Google Scholar 

  • Wang C, Lu J, Zhang S, Wang P, Hou J, Qain J (2011) Effects of Pb stress on nutrient uptake and secondary metabolism in submerged macrophytes Vallisneria natans. Ecotoxicol Environ Saf 74:1297–1303

    CAS  PubMed  Google Scholar 

  • Wang Y, Zhang J, Li JL, Ma XR (2014) Exogenous hydrogen peroxide enhanced the thermo tolerance of Festucaarundinacea and Loliumperenne by increasing the antioxidative capacity. Acta Physiol Plant 36:2915–2924

    CAS  Google Scholar 

  • Wang P, Zhu JK, Lang Z (2015) Nitric oxide suppresses the inhibitory effect of abscisic acid on seed germination by s-nitrosylation of snrk2 proteins. Plant Signal Behav 10:1031939

    Google Scholar 

  • Wu XX, Ding HD, Chen JL, Zhang HJ, Zhu WM (2010) Attenuation of salt-induced changes in photosynthesis by exogenous nitric oxide in tomato (Lycopersicon esculentumMill. L.) seedlings. Afr J Biotechnol 9:7837–7846

    CAS  Google Scholar 

  • Wu XW, Zhu H, Zhang H, Ding Zhang HJ (2011) Exogenous nitric oxide protects against salt induced oxidative stress in the leaves from two genotypes of tomato (Lycopersicum esculentum Mill). Acta Physiol Plant 33:1199–1209

    CAS  Google Scholar 

  • Wu D, Chu HY, Jia LX, Chen KM, Zhao LQ (2015) A feedback inhibition between nitric oxide and hydrogen peroxide in the heat shock pathway in arabidopsis seedlings. Plant Growth Regul 75:503–509

    CAS  Google Scholar 

  • Xiang Z, Jin W, Jing Y, Wang XL, Zhao QP, Kong PT et al (2015) Nitric oxide-associated protein1 (atnoa1) is essential for salicylic acid- induced root waving in Arabidopsis thaliana. New Phytol 207:211–224

    Google Scholar 

  • Yu Y, Yang Z, Guo K, Li Z, Zhou H, Wei Y et al (2015) Oxidative damage induced by heat stress could be relieved by nitric oxide in Trichoderma harzianum LTR-2. Curr Microbiol 70:618–622

    CAS  PubMed  Google Scholar 

  • Zeng CL, Liu L, Wang BR, Wu XM, Zhu Y (2011) Physiological effects of exogenous nitric oxide on Brassica juncea seedlings under NaCl stress. Biol Plant 55(2):345–348

    CAS  Google Scholar 

  • Zhang Y, Wang L, Liu Y, Zhang Q, Wei Q, Zhang W (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224:545–555

    CAS  PubMed  Google Scholar 

  • Zhang F, Wang Y, Yang Y, Wu H, Wang D, Liu J (2007) Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant Cell Environ 30:775–785

    PubMed  Google Scholar 

  • Zhang X, Gao B, Xia H (2014) Effect of cadmium on growth, photosynthesis, mineral nutrition and metal accumulation of banagrass and vetivergrass. Ecotoxicol Environ Saf 106:102–108

    CAS  PubMed  Google Scholar 

  • Zhang L, Li X, Li X, Wei Z, Han M, Zhang L, Li B (2016) Exogenous nitric oxide protects against drought-induced oxidative stress in Malus rootstocks. Truk J Bot 40:17–27

    CAS  Google Scholar 

  • Zhao MG, Tian QY, Zhang WH (2007) Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol 144:206–217

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng C, Jiang D, Liu F, Dai T, Liu W, Jing Q, Cao W (2009) Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environ Exp Bot 67(1):222–227

    CAS  Google Scholar 

  • Zottini M, Formentin E, Scattolin M, Carimi F, Schiavo FL, Terzi M (2002) Nitric oxide affects plant mitochondrial functionality in vivo. FEBS Lett 515:75–78

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors highly acknowledge the Government College University, Faisalabad, Pakistan for its support. The authors would like to extend their sincere appreciation to the Researchers Supporting Project Number (RSP-2021/180), King Saud University, Riyadh, Saudi Arabia.

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SA, MNA, AAA and NH planned the study and QA, NH conducted the experiment, MZH, TJ, and QAl supervised the students during laboratory analysis while MK, NH and QA performed the laboratory analysis, RP and AAA analyzed the data. MNA and SA compiled the whole manuscript.

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Correspondence to Shafaqat Ali.

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Habib, N., Ali, Q., Ali, S. et al. Seed Priming with Sodium Nitroprusside and H2O2 Confers Better Yield in Wheat Under Salinity: Water Relations, Antioxidative Defense Mechanism and Ion Homeostasis. J Plant Growth Regul 40, 2433–2453 (2021). https://doi.org/10.1007/s00344-021-10378-3

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  • DOI: https://doi.org/10.1007/s00344-021-10378-3

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