Skip to main content
Log in

Calcium-Induced Amelioration of Boron Toxicity in Radish

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Like other abiotic stresses, boron (B) toxicity is an important environmental constraint that limits crop productivity worldwide. B toxicity alters many physiological processes necessary for plant survival. The aim of the present study was to investigate the individual and combined effects of calcium (Ca) and B on morphological and physiological attributes of radish (Raphanus sativus L.) under normal and boron-toxicity conditions. The application of 30 mM Ca and 0.5 mM B, alone and in combination, enhanced plant growth, physiological and biochemical attributes. However, 5 mM B was detrimental to most growth and physiological parameters. The application of 30 mM Ca was most effective in alleviating the harmful effects of B toxicity by decreasing malondialdehyde and hydrogen peroxide levels and electrolyte leakage and by enhancing the activities of the antioxidant enzymes superoxide dismutase, catalase, peroxidase, glutathione reductase, and ascorbate peroxidase. Ca clearly induced plant protection mechanisms by enhancing the accumulation of proline, total soluble carbohydrates, and photosynthetic pigments in leaves.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

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

    Article  PubMed  CAS  Google Scholar 

  • Ardıc M, Sekmen AH, Tokur S, Ozdemir F, Turkan I (2009) Antioxidant responses of chickpea plants subjected to boron toxicity. Plant Biol 11:328–338

    Article  PubMed  Google Scholar 

  • Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW (1992) A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environ Exp Bot 32:85–100

    Article  CAS  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 

  • Bolaños L, Lukaszewski K, Bonilla I, Blevins D (2004) Why boron? Plant Physiol Biochem 42:907–912

    Article  PubMed  Google Scholar 

  • Cakmak I, Römheld V (1997) Boron deficiency-induced impairments of cellular functions in plants. Plant Soil 193:71–83

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chance B, Maehly AC (1955) Assay of catalase and peroxidases. Methods Enzymol 2:764–775

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dwivedi RS, Randhawa NS (1974) Evolution of a rapid test for the hidden hunger of zinc in plants. Plant Soil 40:445–451

    Article  CAS  Google Scholar 

  • Fitzpatrick KL, Reid RJ (2009) The involvement of aquaglyceroporins in transport of boron in barley roots. Plant Cell Environ 32:1357–1365

    Article  PubMed  CAS  Google Scholar 

  • Foyer C, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  Google Scholar 

  • Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signaling. New Phytol 146:359–388

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Guimarães FVA, Lacerda CFD, Marques EC, Miranda MRAD, Abreu CEBD, Prisco JT, Gomes-Flho E (2011) Calcium can moderate changes on membrane structure and lipid composition in cowpea plants under salt stress. Plant Growth Regul 65:55–63

    Article  Google Scholar 

  • Gunes A, Soylemezoglu G, Inal A, Bagci EG, Coban S, Sahin O (2006) Antioxidant and stomatal responses of grapevine (Vitis vinifera L.) to boron toxicity. Sci Hortic 110:279–284

    Article  CAS  Google Scholar 

  • Gupta UC (1979) Boron nutrition of crops. Adv Agron 31:273–307

    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  PubMed  CAS  Google Scholar 

  • Herrera-Rodríguez MB, González-Fontes A, Rexach J, Camacho-Cristóbal JJ, Maldonado JM, Navarro-Gochicoa MT (2010) Role of boron in vascular plants and response mechanisms to boron stresses. Plant Stress 4:115–122

    Google Scholar 

  • Hirschi KD (2004) The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol 136:2438–2442

    Article  PubMed  CAS  Google Scholar 

  • Hseu ZY (2004) Evaluating heavy metal contents in nine composts using four digestion methods. Bioresour Technol 95:53–59

    Article  PubMed  CAS  Google Scholar 

  • Iyer S, Caplan A (1998) Products of proline catabolism can induce osmotically regulated genes in rice. Plant Physiol 116:203–211

    Article  CAS  Google Scholar 

  • Kanwak S, Rahmatullah AT, Maqsood MA, Abbas N (2008) Critical ratio of calcium and boron in maize shoot for optimum growth. J Plant Nutr 31:1535–1542

    Article  Google Scholar 

  • Keren R, Bingham FT (1985) Boron in water, soils, and plants. Adv Soil Sci 1:230–276

    Google Scholar 

  • Khan MN, Siddiqui MH, Mohammad F, Naeem M, Khan MMA (2010) Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation. Acta Physiol Plant 32:121–132

    Article  Google Scholar 

  • Kyle DJ (1987) The biochemical basis for photoinhibition of photosystem II. In: Kyle DJ, Osmond CB, Artzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 197–226

    Google Scholar 

  • Liu P, Yang PA (2000) Effects of molybdenum and boron on membrane lipid peroxidation and endogenous protective systems of soybean leaves. Acta Bot Sin 42:461–466

    CAS  Google Scholar 

  • Liu Z, Zhu Q, Tong L (1980) Boron-deficient soils and their distribution in China. Tu Jang Hsuch Pao 17:228–239

    CAS  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1995) Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. J Exp Bot 46:1843–1852

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London

    Google Scholar 

  • Matoh T (1997) Boron in plant cell walls. Plant Soil 193:59–70

    Article  CAS  Google Scholar 

  • Matysik J, Alia, Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532

    CAS  Google Scholar 

  • Meloni DA, Gulotta MR, Martinez CA, Oliva MA (2004) The effect of salt stress on growth, nitrate reduction and proline and glycinebetaine accumulation in Prosopis alba. Braz J Plant Physiol 16:39–46

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nable RO, Banuelos GS, Paull JG (1997) Boron toxicity. Plant Soil 193:181–198

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • O’Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Ann Rev Plant Biol 55:109–139

    Article  Google Scholar 

  • Ölçer H, Kocaçaliskan I (2007) Excess boron reduces polyphenol oxidase activities in embryo and endosperm of maize seed during germination. J Biosci 62:111–115

    Google Scholar 

  • Paull JG (1990) Genetic studies on the tolerance of wheat to high concentrations of boron. Ph.D. Thesis, The University of Adelaide, Adelaide

  • Reid R (2007) Update on boron toxicity and tolerance in plants. In: Xu F, Goldbach HE, Brown PH, Bell RW, Fujiwara T, Hunt CD, Goldberg S, Shi L (eds) Advances in plant and animal nutrition. Springer, Dordrecht, pp 83–90

    Chapter  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 25:1405–1414

    Article  Google Scholar 

  • Rerkasem B, Nirantrayagul S, Jamjod S (2003) Increasing boron efficiency in international bread wheat, durum wheat, triticale and barley germplasm will boost production on soils low in boron. Field Crops Res 86:175–184

    Article  Google Scholar 

  • Shomron N, Ast G (2003) Boric acid reversibly inhibits the second step of pre-mRNA splicing. FEBS 552:219–224

    Article  CAS  Google Scholar 

  • Shorrocks VM (1997) The occurrence and correction of boron deficiency. Plant Soil 193:121–148

    Article  CAS  Google Scholar 

  • Siddiqui MH, Khan MN, Mohammad F, Khan MMA (2008a) Role of nitrogen and gibberellin (GA3) in the regulation of enzyme activities and in osmoprotectant accumulation in Brassica juncea L. under salt stress. J Agron Crop Sci 194:214–224

    Article  CAS  Google Scholar 

  • Siddiqui MH, Mohammad F, Khan MN, Khan MMA (2008b) Cumulative effect of soil and foliar application of nitrogen, phosphorus, and sulfur on growth, physico-biochemical parameters, yield attributes, and fatty acid composition in oil of erucic acid-free rapeseed-mustard genotypes. J Plant Nutr 31:1284–1298

    Article  CAS  Google Scholar 

  • Siddiqui MH, Mohammad F, Khan MN (2009a) Morphological and physiobiochemical characterization of Brassica juncea L. Czern. & Coss. genotypes under salt stress. J Plant Interact 4:67–80

    Article  CAS  Google Scholar 

  • Siddiqui MH, Mohammad F, Khan MN, Naeem M, Khan MMA (2009b) Differential response of salt-sensitive and salt-tolerant Brassica juncea genotypes to N application: enhancement of N-metabolism and anti-oxidative properties in the salt-tolerant type. Plant Stress 3:55–63

    Google Scholar 

  • Siddiqui MH, Mohammad F, Khan MN, Al-Whaibi MH, Bahkali AHA (2010) Nitrogen in relation to photosynthetic capacity and accumulation of osmoprotectant and nutrients in Brassica genotypes grown under salt stress. Agr Sci China 9:671–680

    Article  CAS  Google Scholar 

  • Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L. Protoplasma 248:503–511

    Article  PubMed  CAS  Google Scholar 

  • Siddiqui MH, Mohammad F, Khan MMA, Al-Whaibi MH (2012) Cumulative effect of nitrogen and sulphur on Brassica juncea L. genotypes under NaCl stress. Protoplasma 249:139–153

    Article  PubMed  CAS  Google Scholar 

  • Singh MV (2006) Emerging boron deficiency in soils and crops in India and its management. 18th World Congress of Soil Science, Philadelphia

  • Smith GS, Johnston CM, Cornforth IS (1983) Comparison of nutrient solutions for growth of plants in sand culture. New Phytol 94:537–548

    Article  CAS  Google Scholar 

  • Tombuloglu H, Semizoglu N, Sakcali S, Kekec G (2012) Boron induced expression of some stress-related genes in tomato. Chemosphere 85:433–438

    Article  Google Scholar 

  • Torun AA, Yazici A, Erdem H, Çakmak I (2006) Genotypic variation in tolerance to boron toxicity in 70 durum wheat genotypes. Tur J Agric For 30:49–58

    CAS  Google Scholar 

  • Turan MA, Taban N, Taban S (2009) Effect of calcium on the alleviation of boron toxicity and localization of boron and calcium in cell wall of wheat. Not Bot Hort Agrobot Cluj 37:99–103

    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 

  • Watson DJ (1958) The dependence of net assimilation rate on leaf area index. Ann Bot 22:37–54

    Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511

    Article  PubMed  CAS  Google Scholar 

  • Wise RR, Naylor AW (1987) Chilling-enhanced photo-oxidation. The peroxidation destruction of lipids during chilling injury to photosynthesis and ultrastructure. Plant Physiol 83:278–282

    Article  PubMed  CAS  Google Scholar 

  • Xuan H, Streif J, Pfeffer H, Dannel F, Romheld V, Bangerth F (2001) Effect of pre-harvest boron application on the incidence of CA-storage related disorders in ‘Conference’ pears. J Hort Sci Biotechnol 76:133–137

    CAS  Google Scholar 

  • Yamauchi T, Hara T, Sonoda Y (1986) Distribution of Ca and B in the pectin fraction of tomato leaf cell wall. Plant Cell Physiol 27:727–732

    Google Scholar 

  • Yau SK, Ryan J (2008) Boron toxicity tolerance in crops: a viable alternative to soil amelioration. Crop Sci 48:854–865

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The financial support by the Deanship of Scientific Research of King Saud University, Riyadh, KSA, to the Research Group No. RGPVPP-153 is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Manzer H. Siddiqui.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Siddiqui, M.H., Al-Whaibi, M.H., Sakran, A.M. et al. Calcium-Induced Amelioration of Boron Toxicity in Radish. J Plant Growth Regul 32, 61–71 (2013). https://doi.org/10.1007/s00344-012-9276-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-012-9276-6

Keywords

Navigation