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Hydrogen peroxide supplementation alleviates the deleterious effects of cadmium on photosynthetic pigments and oxidative stress and improves growth, yield and pods quality of pea (Pisum sativum L.) plants

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Abstract

The effects of foliar applied H2O2 on chlorophyll, carotenoids, the non-enzymatic defense system (ascorbic acid), malondialdehyde (MDA) hydrogen peroxide (H2O2) and growth were assessed in roots and shoots of pea (Pisum sativum L.) plants exposed to excess cadmium. In addition, we evaluated the influences of H2O2 spraying on proline, soluble sugars and soluble proteins contents. Excessive cadmium treatment caused reduction in the growth parameters (dry mass, pods and seeds dry weights), chlorophyll and carotenoids contents, roots total free amino acids, roots soluble sugars as well as shoots and roots soluble proteins levels but increased total free amino acids and soluble sugars contents in shoots. Concentrations of hydrogen peroxide and MDA was enhanced under Cd treatment. The foliar treatment of H2O2 alleviated the detrimental effects generated under Cd treatment that represented as increment in pea growth. H2O2 spraying increased photosynthetic pigments, growth characteristics, soluble proteins, and ascorbic acid contents comparing to the control sets not receiving H2O2. Similarly, a higher up-regulation was detected in proline contents of Cd + H2O2 set than Cd group ones at 0.25 mM Cd. Contrarily, malondialdehyde (MDA), soluble sugars and total free amino acids contents of Cd + H2O2 set revealed a lower decrease than Cd group ones especially in roots. The results demonstrated that H2O2 treatment could inverse the harmful effects of cadmium on growth, through inducing the non-enzymatic defense system (ascorbate), proline accumulation, maintenance of chlorophyll in pea leaves and lowering the intensity of H2O2 and lipid peroxidation (MDA).

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Abbreviations

AsA:

Ascorbic acid

Chl:

Chlorophyll

LP:

Lipid peroxidation

GSH:

Glutathione

MDA:

Malondialdehyde

ROS:

Reactive oxygen species

SS:

Soluble sugars

SP:

Soluble proteins

TAA:

Total free amino acids

TCA:

Trichloroacetic acid

References

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

    CAS  Google Scholar 

  • Ahmad P, Sarwat M, Bhat NA, Wani MR, Kazi AG, Tran LP (2015) Alleviation of cadmium toxicity in Brassica juncea L (Czern & Coss) by calcium application involves various physiological and biochemical strategies. PLoS ONE 10(1):e0114571

    Article  PubMed  PubMed Central  Google Scholar 

  • Alloway BJ (2013) Trace metals and metalloids in soils and their bioavailability. Environmental pollution, vol 22, 3rd edn. Springer, Dordrecht

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bienert GP, Schjoerring JK, Jahn TP (2006) Membrane transport of hydrogen peroxide. Biochim Biophys Acta 1758:994–1003

    Article  CAS  PubMed  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt V (2003) Antioxidants, oxidative damage and oxygen deprivation stress. A review. Ann Bot 91:179–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burzynski M, Migocka M, Klobus G (2005) Cu and Cd transport in cucumber (Cucumis sativus L.) root plasma membranes. Plant Sci 168:1609–1614

    Article  CAS  Google Scholar 

  • Chakraborty K, Sairam RK, Bhattacharya RC (2012) Differential expression of salt overly sensitive pathway genes determines salinity stress tolerance in Brassica genotypes. Plant Physiol Biochem 51:90–101

    Article  CAS  PubMed  Google Scholar 

  • Charest C, Phan CT (1990) Cold acclimation of wheat (Triticum aestivum) properties of enzymes involved in proline metabolism. Physiol Plant 80:159–168

    Article  CAS  Google Scholar 

  • Clemens S, Aarts MG, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18(2):92–99

    Article  CAS  PubMed  Google Scholar 

  • DalCorso G, Farinati S, Maistri S, Furini A (2008) How plants cope with cadmium: staking all on metabolism and gene expression. J Integr Plant Biol 50:1268–1280

    Article  CAS  PubMed  Google Scholar 

  • Down RJ, Hellmers H (1975) Environment and experimental control of plant growth. Acad Press, London, New York, San Francisco, p 145

    Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rabers PA, Smith F (1956) Colorimetric method for the determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Duncan DB (1955) Multiple ranges and multiple F-test. Biometrics 11:1–42

    Article  Google Scholar 

  • Gadallah MAA (1995) Effect of cadmium and kinetin on chlorophyll content, saccharides and dry matter accumulation in sunflower plants. Biol Plant 37:233–240

    Article  CAS  Google Scholar 

  • Gadallah MAA (1999) Effects of proline and glycinebetaine on Vicia faba responses to salt stress. Biol Plant 42:249–257

    Article  CAS  Google Scholar 

  • Gadallah MAA, Sayed SA (2014) Impacts of different water pollution sources on antioxidant defense ability in three aquatic macrophytes in Assiut Province, Egypt. J Stress Physiol Biochem 10:47–61

    Google Scholar 

  • Gill M (2014) Heavy metal stress in plants: a review. Int J Adv Res 2(1043):1055

    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 

  • Gondim FA, Gomes-Filho E, Lacerda CF, PriscoJ T, André D, AzevedoNetoA D, Marques EC (2010) Pretreatment with H2O2 in maize seeds: effects on germination and seedling acclimation to salt stress. Braz J Plant Physiol 22:103–112

    Article  Google Scholar 

  • Gondium FA, Miranda RD, 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(4):251–260

    Article  Google Scholar 

  • Gong M, Chen B, Li ZG, Guo LH (2001) Heat-shock-induced cross adaptation to heat, chilling, drought and salt in maize seedlings and involvement of H2O2. J Plant Physiol 158:1125–1130

    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 

  • Guzel S, Terzi R (2013) Exogenous hydrogen peroxide increases dry matter production, mineral content and level of osmotic solutes in young maize leaves and alleviates deleterious effects of copper stress. Bot Stud 54:26

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasanuzzaman M, Nahar K, Gill SS, Alharby HF, Razafindrabe BHN, Fujita M (2017) Hydrogen peroxide pretreatment mitigates cadmium-induced oxidative stress in Brassica napus L.: an intrinsic study on antioxidant defense and glyoxalase systems. Front Plant Sci 8(115):1–10

    Google Scholar 

  • Hooda PS (ed) (2010) Trace elements in soils. Wiley, Chichester

    Google Scholar 

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

    Google Scholar 

  • Hu Y, Ge Y, Zhang C, Ju T, Cheng W (2009) Cadmium toxicity and translocation in rice seedlings are reduced by hydrogen peroxide pretreatment. Plant Growth Reg 59:51–61

    Article  CAS  Google Scholar 

  • Hyat S, Hayat Q, Alyemeni MN, Ahmad A (2013) Proline enhances antioxidative enzyme activity, photosynthesis and yield of Cicer arietinum L. exposed to cadmium stress. Acta Bot Croat 72:323–335

    Article  Google Scholar 

  • Ismail SZ, Khandaker MM, Mat N, Boyce AN (2015) Effects of hydrogen peroxide on growth, development and quality of fruits: a review. J Agron 14(4):331–336

    Article  CAS  Google Scholar 

  • Jackson ML (1967) Soil chemical analysis. New Delhi, Prentice-Hall of India, Private limited New Delhi, p 498

    Google Scholar 

  • Jali P, Pradhan C, Das AB (2016) Effects of cadmium toxicity in plants: a review article. Sch Acad J Biosci 4(12):1074–1081

    CAS  Google Scholar 

  • Kabta-Pendias A (2011) Trace elements in soils and plants. CRC Press, Taylor and Francis Group, Boca Raton

    Google Scholar 

  • Khan DM, Mei L, Ali B, Chen Y, Cheng X, Zhu SJ (2013) Cadmium-induced up regulation of lipid peroxidation and reactive oxygen species caused physiological, biochemical, and ultrastructural changes in upland cotton seedlings. Bio Med Res Int 2013:10

    Google Scholar 

  • Khan A, Anwar Y, Hasan MM, Iqbal A, Ali M, Alharby HF, Hakeem KR, Hasanuzzaman M (2017) Attenuation of drought stress in Brassica seedlings with exogenous application of Ca2+ and H2O2. Plants 6(2):20

    Article  PubMed Central  Google Scholar 

  • Khandaker M, Boyce AN, Osman N (2012) The influence of hydrogen peroxide on the growth, development and quality of wax apple (Syzygium samarangense, [Blume] Merrill and L.M. Perry var. jambumadu) fruits. Plant Physiol Biochem 53:101–110

    Article  CAS  PubMed  Google Scholar 

  • Lee YP, Takahashi T (1966) An improved colorimetric determination of amino acids with the use of ninhydrin. Anal Biochem 14:71–77

    Article  CAS  Google Scholar 

  • Lin Q, Chen Y, Wang Z, Wang Y (2004) Study on the possibility of hydrogen peroxide pretreatment and plant system to remediate soil pollution. Chemosphere 57:1439–1447

    Article  PubMed  Google Scholar 

  • Lowry OH, Resbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin–phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • MadhavaRao KV, Sresty TV (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Migocka M, Papierniak A, Kosatka E, Klobus G (2011) Comparative study of the active cadmium efflux systems operating at the plasma membrane and tonoplast of cucumber root cells. J Exp Bot 62(14):4903–4916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implications of water stress induced changes in the levels of endogenous ascorbic acid and H2O2 in Vigna seedlings. Plant Physiol 58:166–170

    Article  CAS  Google Scholar 

  • Muradoglu F, Gundogdu M, Ercisli S, EncuT Balta F, Jaafar HZE (2015) Cadmium toxicity affects chlorophyll a and b content, antioxidant enzyme activities and mineral nutrient accumulation in strawberry. Biol Res 48:11

    Article  PubMed  PubMed Central  Google Scholar 

  • Nayyar H (2003) Variation in osmoregulation in differentially drought-sensitive wheat genotypes involves calcium. Biologia Plant 47:541–547

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signaling. Curr Opin Plant Biol 5:388–395

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol 49:249–279

    Article  CAS  Google Scholar 

  • Peng Q, Chen W, Wu L, Bai L (2017) The uptake, accumulation, and toxic effects of cadmium in barnyard grass (Echinochloa crusgalli). Pol J Environ Stud 26(2):779–784

    Article  CAS  Google Scholar 

  • Plaza S, Weber J, Pajonk S, Thomas J, Talke IN, Schellenberg M, Pradervand S, Burla B, Geisler M, Martinoia E, Krämer U (2015) Wounding of Arabidopsis halleri leaves enhances cadmium accumulation that acts as a defense against herbivory. Biometals 28(3):521–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shah K, Mankad AU, Reddy MN (2017) Cadmium accumulation and its effects on growth and biochemical parameters in Tagetes erecta L. J Pharmacogn Phytochem 6(3):111–115

    CAS  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 

  • Ślesak I, Libik M, Karpinska B, Karpinski S, Miszalski Z (2007) The role of hydrogen peroxide in regulation of plant metabolism and cellular signalling in response to environmental stresses. Acta Biochim Pol 54:39–50

    PubMed  Google Scholar 

  • Song Y, Miao Y, Song CP (2014) Behind the scenes: the roles of reactive oxygen species in guard cells. New Phytol 201:1121–1140

    Article  CAS  PubMed  Google Scholar 

  • Terzi R, Kadioglua A, Kalaycioglua E, Saglamb 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

    Article  CAS  Google Scholar 

  • Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 163:515–523

    Article  CAS  Google Scholar 

  • Velikova V, Yordanov L, 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 

  • Verbruggen N, Juraniec M, Baliardini C, Meyer CL (2013) Tolerance to cadmium in plants: the special case of hyperaccumulators. Biometals 26(4):633–638

    Article  CAS  PubMed  Google Scholar 

  • Vranová E, Inzé D, Breusegem FV (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236

    Article  PubMed  Google Scholar 

  • Wang Y, Li JL, Wang JZ, Li ZK (2010) Exogenous H2O2improves the chilling tolerance of manila grass and mascarene grass by activating the antioxidative system. Plant Growth Reg 61:195–204

    Article  CAS  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophyll a and b, as well as total caretenoids, using various solvent with spectrophotometers of different solution. J Plant Physiol 144:307–313

    Article  CAS  Google Scholar 

  • Xu FJ, Jin CW, Liu W, Zhang YS, LinX Y (2011) Pretreatment with H2O2 alleviates aluminum-induced oxidative stress in wheat seedlings. J Integr Plant Biol 54:44–53

    Article  Google Scholar 

  • Yang SL, Lan SS, Gong M (2009) Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings. J Plant Physiol 166(15):1694–1699

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We express our gratitude to the respectful reviewers for helpful, purposeful comments to improve the manuscript and present this work in its fullest required form.

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Correspondence to Suzan Sayed.

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Sayed, S., Gadallah, M. Hydrogen peroxide supplementation alleviates the deleterious effects of cadmium on photosynthetic pigments and oxidative stress and improves growth, yield and pods quality of pea (Pisum sativum L.) plants. Acta Physiol Plant 41, 113 (2019). https://doi.org/10.1007/s11738-019-2901-2

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