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Chitosan alleviates phytotoxicity caused by boron through augmented polyamine metabolism and antioxidant activities and reduced boron concentration in Cucumis sativus L.

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Abstract

The aim of this investigation was to study an association among boron-induced oxidative stress, antioxidant system and polyamine metabolism in cucumber Cucumis sativus (L) plants. Furthermore, it was also investigated whether chitosan would increase the antioxidant activity and polyamine concentration that could induce tolerance to boron-induced oxidative stress. Cucumber (cv. Sahil) plants were exposed to 0.5, 1.0, and 1.5 mM boron stress at the 16-day stage for one week while receiving nutrient solution. At the 23- and 27-day stages, plants were foliar-treated with chitosan solution (50 and 75 mg L−1), and harvested at the 34-day stage to investigate growth, photosynthesis, and biochemical characteristics. Boron stress significantly reduced the growth, total chlorophyll concentration, relative water contents, photosynthesis, stomatal conductance, internal CO2 concentration, stomatal size, and membrane stability index. However, boron stress elevated the enzymatic activities of various antioxidants, osmolytes, polyamine concentration, H2O2 concentration, lipid peroxidation and electrolyte leakage in leaves. The follow-up spray with chitosan to the plants subjected to boron stress improved growth, relative water contents, green pigments, photosynthetic activity and membrane stability index, and further enhanced the activity of antioxidant enzymes, osmolytes, leaf polyamine concentration, hydrogen peroxide concentration, lipid peroxidation, and electrolyte leakage in the leaves. The augmented level of antioxidant enzymes, root/shoot osmolytes and leaf polyamine concentration might have induced resistance to the boron stressed plants, causing an ameliorated growth, relative water contents, and photosynthesis related characteristics. It is also concluded that chitosan is an eco-friendly alleviator of toxicity caused by boron by enhancing polyamine concentration and strengthening antioxidant defensive system but reducing the boron concentration in plant tissues.

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References

  • Aftab T, Khan M, Naeem M, Idrees M, Teixeira da Silva JA, Ram M (2012) Exogenous nitric oxide donor protects Artemisia annua from oxidative stress generated by boron and aluminium toxicity. Ecotox Environ Safe 80:60–68

    Article  CAS  Google Scholar 

  • Alcázar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Barrs H, Weatherley P (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Camacho-Cristóbal JJ, Rexach J, González-Fontes A (2008) Boron in plants: deficiency and toxicity. J Integr Plant Biol 50:1247–1255

    Article  PubMed  Google Scholar 

  • Cervilla LM, Blasco B, Ríos JJ, Romero L, Ruiz JM (2007) Oxidative stress and antioxidants in tomato (Solanum lycopersicum) plants subjected to boron toxicity. Ann Bot 100:747–756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chance B, Maehly A (1955) Assay of catalases and peroxidases. Method Enzymol 2:764–775

    Article  Google Scholar 

  • Cvikrova M, Gemperlova L, Dobra J, Martincova O, Prasil IT, Gubis J, Vankova R (2012) Effect of heat stress on polyamine metabolism in proline-over-producing tobacco plants. Plant Sci 182:49–58

    Article  CAS  PubMed  Google Scholar 

  • Esen AHS, Özgür R, Uzilday B, Tanyolaç ZO, Dinc A (2012) The response of the xerophytic plant Gypsophila aucheri to salt and drought stresses: the role of the antioxidant defence system. Turk J Bot 36:697–706

    Google Scholar 

  • Farouk S, Amany AR (2012) Improving growth and yield of cowpea by foliar application of chitosan under water stress. Egypt J Biol 14:14–16

    Google Scholar 

  • Filippou P, Antoniou C, Fotopoulos V (2013) The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. Free Radical Bio Med 56:172–183

    Article  CAS  Google Scholar 

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

    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 

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

    Article  CAS  Google Scholar 

  • Gupta UC (1979) Some factors affecting the determination of hot-water soluble boron from podzol soils using azomethine. Can J Soil Sci 59:241–247

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  PubMed  Google Scholar 

  • Hewitt EJ, Bureaux CA (1996) Sand and water culture methods used in the study of plant nutrition, Cambridge University Press

  • Inal A, Pilbeam DJ, Gunes A (2009) Silicon increases tolerance to boron toxicity and reduces oxidative damage in barley. J Plant Nutr 32:112–128

    Article  CAS  Google Scholar 

  • Ioannidis NE, Kotzabasis K (2007) Effects of polyamines on the functionality of photosynthetic membrane in vivo and in vitro. Biochim Biophys Acta 1767:1372–1382

    Article  CAS  PubMed  Google Scholar 

  • Jiang QQ, Yang HQ, Sun XL, LI Q, Ran K, Zhang XR (2012) Relationship between polyamines metabolism and cell death in roots of Malus hupehensis Rehd. under cadmium stress. J Integr Agri 11:1129–1136

    Article  CAS  Google Scholar 

  • Keles Y, Oncel I, Yenice N (2004) Relationship between boron content and antioxidant compounds in Citrus leaves taken from fields with different water source. Plant Soil 265:345–353

    Article  CAS  Google Scholar 

  • Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381

    Article  CAS  PubMed  Google Scholar 

  • Landi M, Pardossi A, Remorini D, Guidi L (2013) Antioxidant and photosynthetic response of a purple-leaved and a green-leaved cultivar of sweet basil (Ocimum basilicum) to boron excess. Environ Exp Bot 85:64–75

    Article  CAS  Google Scholar 

  • Liu D, Jiang W, Zhang L, Li L (2000) Effects of boron ions on root growth and cell division of broadbean (Vicia faba L.). Isr J Plant Sci 48:47–51

    Article  CAS  Google Scholar 

  • Mahdavi B, Rahimi A (2013) Seed priming with chitosan improves the germination and growth performance of ajowan (Carum copticum) under salt stress. Eur Asi J Bio Sci 7:69–76

    Article  Google Scholar 

  • Masood S, Saleh L, Witzel K, Plieth C, Mühling KH (2012) Determination of oxidative stress in wheat leaves as influenced by boron toxicity and NaCl stress. Plant Physiol Biochem 56:56–61

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mondal M, Malek M, Puteh A, Ismail M, Ashrafuzzaman M, Naher L (2012) Effect of foliar application of chitosan on growth and yield in okra. Aust J Crop Sci 6:918–921

    CAS  Google Scholar 

  • Moya JL, Gómez-Cadenas A, Primo-Millo E, Talon M (2003) Chloride absorption in salt-sensitive Carrizo citrange and salt-tolerant Cleopatra mandarin citrus rootstocks is linked to water use. J Exp Bot 54:825–833

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Papadakis I, Dimassi K, Bosabalidis A, Therios I, Patakas A, Giannakoula A (2004) Effects of B excess on some physiological and anatomical parameters of ‘Navelina’orange plants grafted on two rootstocks. Environ Exp Bot 51:247–257

    Article  CAS  Google Scholar 

  • Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139:487–492

    Article  CAS  PubMed  Google Scholar 

  • Reid R (2007) Update on boron toxicity and tolerance in plants. Advances in plant and animal boron nutrition. Springer, Dordrecht, pp 83–90

    Google Scholar 

  • Reid RJ, Hayes JE, Post A, Stangoulis JCR, Graham RD (2004) A critical analysis of the causes of boron toxicity in plants. Plant, Cell Environ 27:1405–1414

    Article  CAS  Google Scholar 

  • Saha J, Brauer EK, Sengupta A, Popescu SC, Gupta K, Gupta B (2015) Polyamines as redox homeostasis regulators during salt stress in plants. Environ Sci, Front. doi:10.3389/fenvs.2015.00021

    Google Scholar 

  • Shahid MA, Pervez MA, Balal RM, Mattson NS, Rashid A, Ahmad R, Ayyub C, Abbas T (2011) Brassinosteroid (24-epibrassinolide) enhances growth and alleviates the deleterious effects induced by salt stress in pea (Pisum sativum L.). Aust J Crop Sci 5:500–510

    CAS  Google Scholar 

  • Sharma P, Rajam M (1995) Spatial and temporal changes in endogenous polyamine levels associated with somatic embryogenesis from different hypocotyl segments of eggplant (Solanum melongena L.). J Plant Physiol 146:658–664

    Article  CAS  Google Scholar 

  • Shi H, Chan Z (2014) Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. J Intg Plant Biol 56:114–121

    Article  CAS  Google Scholar 

  • Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5, 5′-dithiobis (2-nitrobenzoic acid). Anal Biochem 175:408–413

    Article  CAS  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 

  • Sotiropoulos TE, Molassiotis A, Almaliotis D, Mouhtaridou G, Dimassi K, Therios I, Diamantidis G (2006) Growth, nutritional status, chlorophyll content, and antioxidant responses of the apple rootstock MM 111 shoots cultured under high boron concentrations in vitro. J Plant Nutr 29:575–583

    Article  CAS  Google Scholar 

  • Subhan D, Murthy S (2001) Effect of polyamines on chlorophyll and protein contents, photochemical activity, and energy transfer in detached wheat leaves during dark incubation. Biol Plant 44:529–533

    Article  CAS  Google Scholar 

  • Sullivan CY, Ross W (1979) Selecting for drought and heat resistance in grain sorghum. Stress Physiol Crop Plants 263–281

  • Supanjani LK, Lee K (2006) Hot pepper response to interactive effects of salinity and boron. Plant Soil Environ 52:227–233

    Google Scholar 

  • Tewari AK, Tripathy BC (1998) Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. Plant Physiol 117:851–858

    Article  CAS  Google Scholar 

  • Urbanek H, Kuzniak-Gebarowska E, Herka K (1991) Elicitation of defence responses in bean leaves by Botrytis cinerea polygalacturonase. Acta Physiol Plant 3:34–39

    Google Scholar 

  • Yusuf M, Fariduddin Q, Ahmad A (2011) 28-Homobrassinolide mitigates boron induced toxicity through enhanced antioxidant system in Vigna radiata plants. Chemosphere 85:1574–1584

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The study was executed under the Project No. 20-2315/NRPU/R&D/HEC/12, sponsored by Higher Education Commission of Pakistan (HEC). Therefore, we are very grateful to HEC in this regard.

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Correspondence to Rashad Mukhtar Balal or Muhammad Adnan Shahid.

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Communicated by R. Baczek-Kwinta.

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Balal, R.M., Shahid, M.A., Javaid, M.M. et al. Chitosan alleviates phytotoxicity caused by boron through augmented polyamine metabolism and antioxidant activities and reduced boron concentration in Cucumis sativus L.. Acta Physiol Plant 39, 31 (2017). https://doi.org/10.1007/s11738-016-2335-z

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  • DOI: https://doi.org/10.1007/s11738-016-2335-z

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