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Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato

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Abstract

Experiments were carried out to investigate the role of nitric oxide (NO) in ameliorating the negative effects of cadmium stress in tomato seedlings. Plants treated with cadmium (CdCl2, 150 μM) showed reduced growth, biomass yield, pigment content, chlorophyll fluorescence, and gas exchange parameters. Exogenous application of NO donor (sodium nitroprusside) with nutrient solution protected chlorophyll pigments, restored chlorophyll fluorescence and gas exchange parameters, and caused significant enhancements in growth and biomass yield. Cadmium triggered the synthesis of proline and glycine betaine; however, application of NO caused further enhancement of their accumulation, reflecting an obvious amelioration of the cadmium-induced decline in relative water content. Activities of the antioxidant enzymes superoxide dismutase, catalase, ascorbate peroxidase, and glutathione reductase, monodehydroascorbate reductase, dehydroascorbate reductase, and other enzymatic activities of ascorbate-glutathione cycle were enhanced following the application of NO, as compared with those in untreated seedlings under control and cadmium stress conditions. NO increased the flavonoid and total phenol content in Cd-stressed tomato plants. Moreover, NO application restricted the uptake of cadmium and enhanced the accumulation of nutrients in different parts of tomato plants. On the basis of the findings of the present study, we propose that NO has a potential role as a growth promoter for tomato under cadmium stress.

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References

  • Abd_Allah EF, Hashem A, Alqarawi AA, Alwathnani Hend A (2015) Alleviation of adverse impact of cadmium stress in sunflower (Helianthus annuus L.) by arbuscular mycorrhizal fungi. Pak J Bot 47(2):785–795

  • Aebi H (1984) Catalase in vitro. Method Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Ahanger MA, Agarwal RM, Tomar NS, Shrivastava M (2015) Potassium induces positive changes in nitrogen metabolism and antioxidant system of oat (Avena sativa L cultivar Kent). J Plant Inter 10:211–223

    Google Scholar 

  • Ahanger MA, Moad-Talab N, Abd-Allah EF, Ahmad P, Hajiboland R (2016) Plant growth under drought stress: significance of mineral nutrients. In “Water stress and crop plants: a sustainable approach.” Ed. Ahmad P. Wiley Blackwell. pp. 649–668

  • Ahanger MA, Tyagi SR, Wani MR, Ahmad P (2014) Drought tolerance: roles of organic osmolytes, growth regulators and mineral nutrients. In: Ahmad P, Wani MR (eds) Physiological mechanisms and adaptation strategies in plants under changing environment, vol I. Springer, New York, pp 25–56

    Chapter  Google Scholar 

  • Ahmad P, Abdel Latef AA, Hashem A, Abd Allah EF, Gucel S, Tran L-SP (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347

    PubMed  PubMed Central  Google Scholar 

  • Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of Enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30(3):161–175

  • Ahmad P, Nabi G, Ashraf M (2011) Cadmium-induced oxidative damage in mustard [(Brassica juncea L.) Czern. & Coss.] plants can be alleviated by salicylic acid. South Afri J Bot 77:36–44

    Article  CAS  Google Scholar 

  • Ahmad P, Sarwat M, Bhat NA, Wani MR, Kazi AG, Tran LS (2015) Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PLoS One 10(1):e0114571n.d.

  • Ahmad P, Sharma S (2008) Salt stress and phyto-biochemical responses of plants – a review. Plant Soil Environ 54(3):89–99

    Google Scholar 

  • Anjum NA, Umar S, Iqbal M, Khan NA (2011) Cadmium causes oxidative stress in mung bean [Vigna radiata (L.) Wilczek] by affecting antioxidant enzyme systems and ascorbate-glutathione cycle metabolism. Russ J Plant Physiol 58:92–99

    Article  CAS  Google Scholar 

  • Anjum SA, Tanveer M, Hussain S, Ashraf U, Khan I, Wang L (2017) Alteration in growth, leaf gas exchange, and photosynthetic pigments of maize plants under combined cadmium and arsenic stress. Water Air Soil Pollut 228:13

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts, polyphenol oxidase in Beta vulgaris L. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asgher M, Khan NA, Khan MIR, Fatma M, Masood A (2014) Ethylene production is associated with alleviation of cadmium-induced oxidative stress by sulfur in mustard types differing in ethylene sensitivity. Ecotoxicol Environ Safety 106:54–61

  • Bai XY, Dong YJ, Xu LL, Kong J, Liu S (2015) Effects of exogenous nitric oxide on physiological characteristics of perennial ryegrass under cadmium and copper stress. Russ J Plant Physiol 62(2):237–245

    Article  CAS  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Basalah MO, Ali HM, Al-Whaibi MH, Siddiqui MH, Sakran AM, Al Sahli AA (2013) Nitric oxide and salicylic acid mitigate cadmium stress in wheat seedlings. J Pure Appl Microbiol 7:139–148

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, Pugin A, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burzyński M, Kolano E (2003) In vivo and in vitro effects of copper and cadmium on the plasma membrane H+-ATPase from cucumber (Cucumis sativus L.) and maize (Zea mays L.) roots. Acta Physiol Plant 25:39–45

    Article  Google Scholar 

  • Chesnin L, Yien CH (1950) Turbidimetric determination of available sulfates. Proc Soil Sci Soc Am J 15:149–151

    Article  Google Scholar 

  • Conklin PL, Last RL (1995) Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol 109:203–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Correa-Aragunde N, Lombardo C, Lamattina L (2008) Nitric oxide: an active nitrogen molecule that modulates cellulose synthesis in tomato roots. New Phytol 179:386–396

    Article  CAS  PubMed  Google Scholar 

  • Courtois C, Besson A, Dahan J, Bourque S, Dobrowolska G, Pugin A, Wendehenne D (2008) Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases. J Exp Bot 59:155–163

    Article  CAS  PubMed  Google Scholar 

  • Cui XM, Zhang YK, Wu XB, Liu CS (2010) The investigation of the alleviated effect of copper toxicity by exogenous nitric oxide in tomato plants. Plant Soil Environ 56:274–281

    CAS  Google Scholar 

  • Cummins I, Cole DJ, Edwards R (1999) A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J 18:285–292

    Article  CAS  PubMed  Google Scholar 

  • Cuypers A, Smeets K, Ruytinx J, Opdenakker K, Keunen E, Remans T, Horemans N, Vanhoudt N, Van Sanden S, Van Belleghem F, Guisez Y, Colpaert J, Vangronsveld J (2011) The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol 168:309–316

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Mendoza D, Gil FEY, Santamaria JM, Zapata-Perez O (2007) Multiple effects of cadmium on the photosynthetic apparatus of Avicennia germinans L. as probed by OJIP chlorophyll fluorescence measurements. Z Naturforschung C 62:265–272

    CAS  Google Scholar 

  • Dhindsa RS, Matowe W (1981) Drought tolerance in two mosses: correlated with enzymatic defense against lipid peroxidation. J Exp Bot 32:79–91

    Article  CAS  Google Scholar 

  • Dias MC, Monteiro C, Moutinho-Pereira J, Correia C, Goncalves B, Santos C (2013) Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiol Plant 35:1281–1289

    Article  CAS  Google Scholar 

  • Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    Article  CAS  Google Scholar 

  • Dong Y, Xu L, Wang Q, Fan Z, Kong J, Bai X (2014a) Effects of exogenous nitric oxide on photosynthesis, antioxidative ability, and mineral element contents of perennial ryegrass under copper stress. J Plant Interact 9:402–411

    Article  CAS  Google Scholar 

  • Dong YJ, Jinc SS, Liu S, Xu LL, Kong J (2014b) Effects of exogenous nitric oxide on growth of cotton seedlings under NaCl stress. J Soil Sci Plant Nutr 14:1–13

    Google Scholar 

  • Ehlert C, Maurel C, Tardieu F, Simonneau T (2009) Aquaporin mediated reduction in maize root hydraulic conductivity impacts cell turgor and leaf elongation even without changing transpiration. Plant Physiol 150:1093–1104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ezaki B, Katsuhara M, Kawamura M, Matsumoto H (2001) Different mechanisms of four aluminum (Al)-resistant transgenes for Al toxicity in Arabidopsis. Plant Physiol 127:918–927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farooq M, Basra SMA, Wahid A, Rehman H (2009) Exogenously applied nitric oxide enhances the drought tolerance in fine grain aromatic rice (Oryza sativa L.) J Agro Crop Sci 195:254–261

    Article  CAS  Google Scholar 

  • Fatma M, Khan NA (2014) Nitric oxide protects photosynthetic capacity inhibition by salinity in Indian mustard. J Funct Environ Bot 4(2):106–116

    Article  Google Scholar 

  • Fatma M, Masood A, Per TS, Khan NA (2016) Nitric oxide alleviates salt stress inhibited photosynthetic performance by interacting with sulfur assimilation in mustard. Front Plant Sci 7:521

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernández-Marcos M, Sanz L, Lewis DR, Muday GK, Lorenzo O (2011) Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proc Natl Acad Sci U S A 108:18506–18511

    Article  PubMed  PubMed Central  Google Scholar 

  • Foster JG, Hess JL (1980) Responses of superoxide dismutase and glutathione reductase activities in cotton leaf tissue exposed to an atmosphere enriched in oxygen. Plant Physiol 66:482–487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franklin LA, Levavasseur G, Osmond CB, Henley WJ, Ramus J (1992) Two components of onset and recovery during photoinhibition of Ulva rotundata. Planta 186:399–408

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Hasanuzzaman M, Nahar K, Tuteja N (2013) Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63:254–261

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Gomes MP, Marques TCLLSM, Soares AM (2013) Cadmium effects on mineral nutrition of the Cd-hyperaccumulator Pfaffia glomerata. Biologia 68(2):223–230

    Article  CAS  Google Scholar 

  • Gonçalves JF, Antes FG, Maldaner J, Pereira LB, Tabaldi LA, Rauber R, Rossato LV, Bisognin DA, Dressler VL, Flores EM, Nicoloso FT (2009) Cadmium and mineral nutrient accumulation in potato plantlets grown under cadmium stress in two different experimental culture conditions. Plant Physiol Biochem 47:814–821

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Groppa MD, Ianuzzo MP, Rosales EP, Vazquez SC, Benavides MP (2012) Cadmium modulates NADPH oxidase activity and expression in sunflower leaves. Biol Plant 56:167–171

    Article  CAS  Google Scholar 

  • Hameed A, Rasool S, Azooz MM, Hossain MA, Ahanger MA, Ahmad P (2016) Heavy Metal Stress: Plant Responses and Signaling. In: Ahmad P (ed) Plant metal interaction: Emerging remediation techniques, Elsevier Academic Press. pp. 557–584

  • Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22:584–596

    Article  CAS  PubMed  Google Scholar 

  • He JY, Ren YF, Zhu C, Yan YP, Jiang DA (2008) Effect of Cd on growth, photosynthetic gas exchange, and chlorophyll fluorescence of wild and Cd-sensitive mutant rice. Photosynthetica 46:466–470

    Article  CAS  Google Scholar 

  • Hermes VS, Dall’asta P, Amaral FP, Anacleto KB, Arisi ACM (2013) The regulation of transcription of genes related to oxidative stress and glutathione synthesis in Zea mays leaves by nitric oxide. Biol Plant 57:620–626

    Article  CAS  Google Scholar 

  • Horiguchi H, Aoshima K, Oguma R, Sasaki S, Miyamoto K, Hosoi Y, Katoh T, Kayam F (2010) Latest status of cadmium accumulation and its effects on kidneys, bone, and erythropoiesis in inhabitants of the formerly cadmium-polluted Jinzu River Basin in Toyama, Japan, after restoration of rice paddies. Int Arch Occup Environ Health 83:953–970

    Article  CAS  PubMed  Google Scholar 

  • Hossain Z, Mandal AKA, Datta SK, Biswas AK (2006) Isolation of a NaCl tolerant mutant of Chrysanthemum morifolium by gamma radiation: in vitro mutagenesis and selection by salt stress. Funct Plant Biol 33:91–101

    Article  CAS  Google Scholar 

  • Huang C, He W, Guo J, Chang X, Su P, Zhang L (2005) Increasedsensitivity to salt stress in ascorbate-deficient Arabidopsis mutant. J Exp Bot 56:3041–3049

    Article  CAS  PubMed  Google Scholar 

  • Iqbal N, Umar S, Khan NA (2015) Nitrogen availability regulates proline and ethylene production and alleviates salinity stress in mustard (Brassica juncea). J Plant Physiol 178:84–91

  • Irfan M, Ahmad A, Hayat S (2014) Effect of cadmium on the growth and antioxidant enzymes in two varieties of Brassica juncea. Saudi J Biol Sci 21:125–131

    Article  CAS  PubMed  Google Scholar 

  • John R, Ahmad P, Gadgil K, Sharma S (2009) Cadmium and lead-induced changes in lipid peroxidation, antioxidative enzymes and metal accumulation in Brassica juncea L. at three different growth stages. Arch Agron Soil Sci 55(4):395–405

    Article  CAS  Google Scholar 

  • Jung C, Maeder V, Funk F, Frey B, Sticher H, Frosserd E (2003) Release of phenols from Lupinus albus L. roots exposed to Cu and their possible role in Cu detoxification. Plant Soil 252(2):301–312

  • Kapoor D, Kaur S, Bhardwaj R (2014) Physiological and biochemical changes in Brassica juncea Plants under Cd-induced stress. Biomed Res Int 2014:726070

  • Karcz W, Kurtyka R (2007) Effect of cadmium on growth, proton extrusion and membrane potential in maize coleoptile segments. Biol Plant 51:713–719

    Article  CAS  Google Scholar 

  • 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

  • Kaya C, Ashraf M (2015) Exogenous application of nitric oxide promotes growth and oxidative defense system in highly boron stressed tomato plants bearing fruit. Sci Hort 185:43–47

    Article  CAS  Google Scholar 

  • Khairy AIH, Oh MJ, Lee SM, Kim DS, Roh KS (2016) Nitric oxide overcomes Cd and Cu toxicity in in vitro-grown tobacco plants through increasing contents and activities of rubisco and rubisco activase. Biochimie Open 2:41–51

    Article  Google Scholar 

  • Khan MIR, Nazir F, Asgher M, Per TS, Khan NA (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173:9–18

    Article  CAS  PubMed  Google Scholar 

  • Khan MN, Siddiqui MH, Mohammad F, Naeem M (2012) Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide 27:210–218

    Article  CAS  PubMed  Google Scholar 

  • Khan NA, Asgher M, Per TS, Masood A, Fatma M, Khan MIR (2016) Ethylene potentiates sulfur-mediated reversal of cadmium inhibited photosynthetic responses in mustard. Front Plant Sci 7:1628

  • Kishor PBK, Sangam S, Amrutha RN, Sri Laxmi P, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438

    CAS  Google Scholar 

  • Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330

    Article  CAS  Google Scholar 

  • Leshem YY, Haramaty E (1996) Plant aging: the emission of NO and ethylene and effect of NO-releasing compounds on growth of pea (Pisum sativum) foliage. J Plant Physiol 148:258–263

    Article  CAS  Google Scholar 

  • Li P, Cai R, Gao H, Peng T, Wang Z (2007) Partitioning of excitation energy in two wheat cultivars with different grain protein contents grown under three nitrogen applications in the field. Physiol Plant 129:822–829

    Article  CAS  Google Scholar 

  • Li Q, Lu Y, Shil Y, Wang T, Ni K, Xu L, Liu S, Wang L, Xiong Q, Giesy JP (2013) Combined effects of cadmium and fluoranthene on germination, growth and photosynthesis of soybean seedlings. J Environ Sci 25(9):1936–1946

    Article  CAS  Google Scholar 

  • Li S, Yang W, Yang T, Chen Y, Ni W (2015) Effects of cadmium stress on leaf chlorophyll fluorescence and photosynthesis of Elsholtzia argyi—a cadmium accumulating plant. Int J Phytoremed 17:85–92

    Article  CAS  Google Scholar 

  • Liu S, Yang R, Pan Y, Ma M, Pan J, Zhao Y, Cheng Q, Wu M, Wang M, Zhang L (2015) Nitric oxide contributes to minerals absorption, proton pumps and hormone equilibrium under cadmium excess in Trifolium repens L. plants. Ecotoxicol Environ Saf 119:35–46

    Article  CAS  PubMed  Google Scholar 

  • Lombardo MC, Graziano M, Polacco JC, Lamattina L (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Signal Behav 1:28–33

    Article  PubMed  PubMed Central  Google Scholar 

  • Lopes GKB, Shulman HM, Hermes-Lima M (1999) Polyphenol tannic acid inhibits hydroxyl radical formation from Fenton reaction by complexing ferrous ions. Biochim Biophys Acta/GS 1472:142–152

  • Macri F, Braidot E, Petrusa E, Vianello A (1994) Lipoxygenase activity associated to isolated soybean plasma membranes. Biochim Biophys Acta 1215:109–114

    Article  CAS  PubMed  Google Scholar 

  • Madhava Rao KV, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeon pea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  CAS  PubMed  Google Scholar 

  • Mallick N, Mohn FH (2003) Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus. Ecotoxicol Environ Saf 55:64–69

    Article  CAS  PubMed  Google Scholar 

  • Márquez-García B, Ángeles Fernández-Recamales M, Córdoba F (2012) Effects of cadmium on phenolic composition and antioxidant activities of Erica andevalensis. J Bot 2012:936950

  • Melo LCA, Alleoni LRF, Carvalho G, Azevedo RA (2011) Cadmium- and barium-toxicity effects on growth and antioxidant capacity of soybean (Glycine max L.) plants, grown in two soil types with different physicochemical properties. J Plant Nutr Soil Sci 1–13

  • Mendoza-Cozatl D, Loza-Tavera H, Hernandez-Navarro A, Moreno-Sanchez R (2005) Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiol Rev 29:653–671

    Article  CAS  PubMed  Google Scholar 

  • Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish J Environ Studies 15:523–530

  • Miyake C, Asada K (1992) Thylakoid bound ascorbate peroxidase in spinach chloroplast and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol 33:541–553

    CAS  Google Scholar 

  • Mostofa MG, Seraj ZI, Fujita M (2014) Exogenous sodium nitroprusside and glutathione alleviate copper toxicity by reducing copper uptake and oxidative damage in rice (Oryza sativa L.) seedlings. Protoplasma 251:1373–1386

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplast. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nazar R, Iqbal N, Masood A, Khan MIR, Syeed S, Khan NA (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. Am J Plant Sci 3:1476–1489

    Article  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lombardo MC, Lamattina L (2004) Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135:279–286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Per TS, Khan NA, Masood A, Fatma M (2016) Methyl jasmonate alleviates cadmiuminduced photosynthetic damages through increased S-assimilation and glutathione production in mustard. Front Plant Sci 7:1933

  • Pietrini F, Bianconi D, Massacci A, Iannelli MA (2016) Combined effects of elevated CO2 and Cd-contaminated water on growth, photosynthetic response, Cd accumulation and thiolic components status in Lemna minor L. J Hazard Mater 309:77–86

    Article  CAS  PubMed  Google Scholar 

  • Roxas VP, Smith RK, Allen ER, Allen RD (1997) Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15:988–991

    Article  CAS  PubMed  Google Scholar 

  • Shan S, Liu F, Li C (2012) Effects of cadmium on growth, oxidative stress and antioxidant enzyme activities in peanut (Arachis hypogaea L.) seedlings. J Agric Sci 4(6):142–151

    Google Scholar 

  • Shao HB, Chu LY, Zhao HL, Kang C (2008) Primary antioxidant free radical scavenging and redox signalling pathways in higher plant cells. Int J Biol Sci 4:8–14

    Article  CAS  Google Scholar 

  • Simontacchi M, Galatro A, Ramos-Artuso F, Santa-María GE (2015) Plant survival in a changing environment: the role of nitric oxide in plant responses to abiotic stress. Front Plant Sci 6:977

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh A, Prasad SM (2014) Effect of agro-industrial waste amendment on Cd uptake in Amaranthus caudatus grown under contaminated soil: an oxidative biomarker response. Ecotoxicol Environ Saf 100:105–113

    Article  CAS  PubMed  Google Scholar 

  • Singh HP, Kaur S, Batish DR, Sharma 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

    Article  CAS  PubMed  Google Scholar 

  • Sun C, Liu L, Yu Y, Liu W, Lu L, Jin C, Lin X (2015) Nitric oxide alleviates aluminum-induced oxidative damage through regulating the ascorbate-glutathione cycle in roots of wheat. J Integr Plant Biol 57:550–561

    Article  CAS  PubMed  Google Scholar 

  • Tossi V, Amenta M, Lamattina L, Cassia R (2011) Nitric oxide enhances plant ultraviolet-B protection up-regulating gene expression of the phenylpropanoid biosynthetic pathway. Plant Cell Environ 34:909–921

    Article  CAS  PubMed  Google Scholar 

  • Vassilev A, Nikolova A, Koleva L, Lidon F (2011) Effects of excess Zn on growth and photosynthetic performance of young bean plants. J Phytol 3:58–62

    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 polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Wang QH, Liang X, Dong YJ, Xu LL, Zhang XW, Hou J, Fan ZY (2013) Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass. Plant Growth Regul 69:11–20

    Article  CAS  Google Scholar 

  • Wang Z, Li Q, Wu W, Guo J, Yang Y (2017) Cadmium stress tolerance in wheat seedlings induced by ascorbic acid was mediated by NO signaling pathways. Ecotoxicol Environ Saf 135:75–81

    Article  CAS  PubMed  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. a colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

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

    Article  CAS  Google Scholar 

  • Wu Y, Wang WX (2011) Accumulation subcellular distribution and toxicity of inorganic mercury and methyl mercury in marine phytoplankton. Environ Pollut 159:3097–3105

    Article  CAS  PubMed  Google Scholar 

  • Wu Z, Zhao X, Sun X, Tan Q, Tang Y, Nie Z, Qu C, Chen Z, Hu C (2015) Antioxidant enzyme systems and the ascorbate–glutathione cycle as contributing factors to cadmium accumulation and tolerance in two oilseed rape cultivars (Brassica napus L.) under moderate cadmium stress. Chemosphere 138:526–536

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, An LY, Lu H, Zhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, Fu G, Tao L, Zhu C (2010) Roles of nitric oxide in alleviating heavy metal toxicity in plants. Arch Biochem Biophys 497:13–20

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Wang W, Yin H, Liu X, Sun H, Mi Q (2010) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321–330

    Article  CAS  Google Scholar 

  • Xu LL, Fan ZY, Dong YJ, Kong J, Bai XY (2015) Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of two peanut cultivars under cadmium stress. Biol Plant 59:171–182

    Article  CAS  Google Scholar 

  • Yamasaki S, Dillenburg LC (1999) Measurements of leaf relative water content in Araucaria angustifolia. Rev Bras Fisiol Veg 11:69–75

    Google Scholar 

  • Yin L, Wang S, Eltayeb AE, Uddin MI, Yamamoto Y, Tsuji W, Takeuchi Y, Tanaka K (2010) Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231:609–621

    Article  CAS  PubMed  Google Scholar 

  • Yu CW, Murphy TM, Lin CH (2003) Hydrogen peroxide–induces chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol 30:955–963

    Article  CAS  Google Scholar 

  • Zhang J, Chen J, Hu Y, Mo Y (2007) Effects of cadmium stress on photosynthetic function of leaves of Lemna minor L. J Agro-Environ Sci 6:2027–2032

    Google Scholar 

  • Zhang L, Wang Y, Zhao L, Shi S, Zhang L (2006) Involvement of nitric oxide in light-mediated greening of barley seedlings. J Plant Physiol 163:818–826

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Jin Q, Wang Y, Chu L, Li X, Xu Y (2016) Effects of nitric oxide on alleviating cadmium stress in Typha angustifolia. Plant Growth Regul 78:243–251

    Article  CAS  Google Scholar 

  • Zoffoli HJ, do Amaral-Sobrinho NM, Zonta E, Luisi MV, Marcon G, Tolon Becerra A (2013) Inputs of heavy metals due to agrochemical use in tobacco fields in Brazil’s southern region. Environ Monit Assess 185:2423–2437

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to extend their sincere appreciation to the Deanship of Scientific Research at King Saud University for funding this research group (no. RG-1438-039).

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Authors and Affiliations

  1. Department of Botany and Microbiology, Faculty of Science, King Saud University, Riyadh, 11451, Saudi Arabia

    Parvaiz Ahmad, Mohammed Nasser Alyemeni & Leonard Wijaya

  2. Department of Botany, S.P. College, Srinagar, Jammu and Kashmir, 190001, India

    Parvaiz Ahmad

  3. Stress Physiology Laboratory, Department of Botany, Jiwaji University Gwalior, Gwalior, MP, 474011, India

    Mohammed Abass Ahanger

  4. Biology Department, College of Science and Humanities, Prince Sattam bin Abdulaziz University (PSAU), 11942, Alkharj, Kingdom of Saudi Arabia

    Pravej Alam

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  1. Parvaiz Ahmad
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  2. Mohammed Abass Ahanger
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  3. Mohammed Nasser Alyemeni
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  4. Leonard Wijaya
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  5. Pravej Alam
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Correspondence to Parvaiz Ahmad.

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Ahmad, P., Ahanger, M.A., Alyemeni, M.N. et al. Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato. Protoplasma 255, 79–93 (2018). https://doi.org/10.1007/s00709-017-1132-x

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  • DOI: https://doi.org/10.1007/s00709-017-1132-x

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