Skip to main content
SpringerLink
Log in

Interaction of boron and aluminum on the physiological characteristics of rape (Brassica napus L.) seedlings

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

It has been reported that aluminum (Al) toxicity is a major limiting factor for plant growth and production on acidic soils. Boron (B) is indispensable micronutrient for normal growth of higher plants, and its addition could alleviate Al toxicity. The rape seedlings were grown under three B (0.25, 25 and 500 μM) and two Al concentrations [0 (−Al) and 100 μM (+Al) as AlCl3·6H2O]. The results indicated that Al stress severely hampered root elongation and root activity at 0.25 μM B while the normal (25 μM) and excess (500 μM) B improved the biomass of rape seedlings under Al exposure. Additionally, normal and excess B treatment reduced accumulation of Al in the roots and leaves under Al toxicity, which was also confirmed by hematoxylin with light staining. This indicates that both normal and excess B could alleviate Al toxicity. Furthermore, it also decreased the contents of malondialdehyde and soluble protein under Al toxicity. Likewise, superoxide dismutase activity (SOD) improved by 97.82 and 131.96% in the roots, and 168 and 119.88% in the leaves at 25 and 500 µM B, respectively, while the peroxidase and catalase activities dropped as a result of Al stress. The study results demonstrated that appropriate B application is necessary to avoid the harmful consequences of Al toxicity in rape seedlings.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Achary VM, Jena S, Panda KK, Panda BB (2008) Aluminium-induced oxidative stress and DNA damage in root cells of Allium cepa L. Ecotoxicol Environ Saf 70:300–310

    Article  CAS  PubMed  Google Scholar 

  • Aebi H (1983) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analyses verlag nodulation of neuronal excitability by NO. Trends Neurosci 25:510–517

  • Ashraf M, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Bai B, Jin J, Huang L, Bai S (1994) Improvement of TTC method determining root activity in corn. Maizeence 4:44–47 (in Chinese with English abstract)

    Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Blamey F, Edwards D, Asher C (1983) Effects of aluminum, OH:Al and P:Al molar ratios, and ionic strength on soybean root elongation in solution culture. Soil Sci 136:197–207

    Article  CAS  Google Scholar 

  • Blevins DG, Lukaszewski KM (1998) Boron in plant structure and function. Annu Rev Plant Physiol Plant Mol Biol 49:481–500

    Article  CAS  PubMed  Google Scholar 

  • Brown PH, Hu H (1997) Does boron play only a structural role in the growing tissues of higher plants? Plant Soil 196:211–215

    Article  CAS  Google Scholar 

  • Brown PH, Bellaloui N, Wimmer MA, Bassil ES, Ruiz J, Hu H, Pfeffer H, Dannel F, Roemheld V (2002) Boron in plant biology. Plant Biology 4:205–223

    Article  CAS  Google Scholar 

  • Cai K, Gao D, Luo S, Zeng R, Yang J, Zhu X (2008) Physiological and cytological mechanisms of silicon-induced resistance in rice against blast disease. Physiol Plant 134:324–333

    Article  CAS  PubMed  Google Scholar 

  • Chang Y, Yamamoto Y, Matsumoto H (1999) Accumulation of aluminium in the cell wall pectin in cultured tobacco (Nicotiana tabacum L.) cells treated with a combination of aluminium and iron. Plant Cell Environ 22:1009–1017

    Article  CAS  Google Scholar 

  • Chen Q, Chen L, Wu K, Li K, Yu Y (2012) Research progresses in plant aluminum-responsive genes. J Plant Genet Resour 13:858–864

    CAS  Google Scholar 

  • Corrales I, Poschenrieder C, Barceló J (2008) Boron-induced amelioration of aluminum toxicity in a monocot and a dicot species. J Plant Physiol 165:504–513

    Article  CAS  PubMed  Google Scholar 

  • Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dible W, Truog E, Berger K (1954) Boron determination in soils and plants. Anal Chem 26:186–196

    Article  Google Scholar 

  • Dong B, Sang W, Jiang X, Zhou J, Kong F, Hu W, Wang L (2002) Effects of aluminum on physiological metabolism and antioxidant system of wheat (Triticum aestivum L). Chemosphere 47:87–92

    Article  CAS  PubMed  Google Scholar 

  • Franco CR, Chagas AP, Jorge RA (2002) Ion-exchange equilibria with aluminum pectinates. Colloids Surf A 204:183–192

    Article  CAS  Google Scholar 

  • Goldbach HE, Huang L, Wimmer MA (2007) Boron functions in plants and animals: recent advances in boron research and open questions, Advances in plant and animal boron nutrition. Springer, Amsterdam, pp 3–25

    Google Scholar 

  • Goldberg S (1997) Reactions of boron with soils. Plant Soil 193:35–48

    Article  CAS  Google Scholar 

  • Gunes A, Alpaslan M, Cikili Y, Ozcan H (1999) Effect of zinc on the alleviation of boron toxicity in tomato. J Plant Nutr 22:1061–1068

    Article  CAS  Google Scholar 

  • Guo T, Zhang G, Zhou M, Wu F, Chen J (2004) Effects of aluminum and cadmium toxicity on growth and antioxidant enzyme activities of two barley genotypes with different Al resistance. Plant Soil 258:241–248

    Article  CAS  Google Scholar 

  • Guo T, Chen Y, Zhang Y, Jin Y (2006) Alleviation of Al toxicity in barley by addition of calcium. Agric Sci China 5:828–833

    Article  CAS  Google Scholar 

  • Heidarabadi MD, Ghanati F, Fujiwara T (2011) Interaction between boron and aluminum and their effects on phenolic metabolism of Linum usitatissimum L. roots. Plant Physiol Biochem 49:1377–1383

    Article  PubMed  Google Scholar 

  • Horst WJ, Wang Y, Eticha D (2010) The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann Bot 106:185–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu H, Brown PH, Labavitch JM (1996) Species variability in boron requirement is correlated with cell wall pectin. J Exp Bot 47:227–232

    Article  CAS  Google Scholar 

  • Huang X, Li Y, Dong D (2009) Comparison of reactive oxygen metabolism in response to phosphorus deficiency and aluminum toxicity in two contrasting soybean genotypes. Southwest China J Agric Sci 22:615–620

    Google Scholar 

  • Islam E, Yang X, Li T, Liu D, Jin X, Meng F (2007) Effect of Pb toxicity on root morphology, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 147:806–816

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Tang N, Zheng J, Chen L (2009) Antagonistic actions of boron against inhibitory effects of aluminum toxicity on growth, CO2 assimilation, ribulose-1, 5-bisphosphate carboxylase/oxygenase, and photosynthetic electron transport probed by the JIP test, of Citrus grandis seedlings. BMC Plant Biol 9:102–118

    Article  PubMed  PubMed Central  Google Scholar 

  • Kinraide TB (1991) Identity of the rhizotoxic aluminium species. Plant Soil 134:167–178

    Article  CAS  Google Scholar 

  • Kobayashi M, Nakagawa H, Asaka T, Matoh T, Kobayashi M (1999) Borate-rhamnogalacturonan II bonding reinforced by Ca2+ retains pectic polysaccharides in higher-plant cell walls. Plant Physiol 119:199–203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee DH, Kim YS, Lee CB (2001) The inductive responses of the antioxidant enzymes by salt stress in the rice (Oryza sativa L.). J Plant Physiol 158:737–745

    Article  CAS  Google Scholar 

  • Lenoble M, Blevins D, Sharp R, Cumbic B (1996) Prevention of aluminum toxicity with supplemental boron I. Maintenance of root elongation and cellular structure. Plant Cell Environ 19:1132–1142

    Article  CAS  Google Scholar 

  • Li M, Yu M (2013) Characteristics of adsorption and desorption of aluminum in pectin as influenced by boron. Sci Agric Sin 46:1595–1602

    CAS  Google Scholar 

  • Li X, Liu J, Fang J, Tao L, Shen R, Li Y, Xiao H, Feng Y, Wen H, Guan J, Wu L, He Y, Goldbach H, Yu M (2017) Boron supply enhances aluminum tolerance in root border cells of pea (Pisum sativum) by interacting with cell wall pectins. Front Plant Sci 8:742

    Article  PubMed  PubMed Central  Google Scholar 

  • Loomis WD, Drust R (1992) Chemistry and biology of boron. Biofactors (Oxford, England) 3:229–239

    CAS  Google Scholar 

  • Ma J, Furukawa J (2003) Recent progress in the research of external Al detoxification in higher plants: a minireview. J Inorg Biochem 97:46–51

    Article  CAS  PubMed  Google Scholar 

  • Malekzadeh P, Mehr RS, Hatamnia AA (2015) Effects of aluminum toxicity on maize (Zea mays L.) seedlings. Iran J Plant Physiol 5:1289–1296

    Google Scholar 

  • Manov GG, Bates RG, Hamer WJ, Acre SF (2002) Values of the constants in the Debye—Hückel equation for activity coefficients. J Am Chem Soc 86:1433–1441

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Matoh T, Kobayashi M (1998) Boron and calcium, essential inorganic constituents of pectic polysaccharides in higher plant cell walls. J Plant Res 111:179–190

    Article  CAS  Google Scholar 

  • Mizuno M, Kamei M, Tsuchida H (1998) Ascorbate peroxidase and catalase cooperate for protection against hydrogen peroxide generated in potato tubers during low-temperature storage. IUBMB Life 44:717–726

    Article  CAS  Google Scholar 

  • O’Neill MA, Ederhard S, Albersheim P, Darvill AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294:846–849

    Article  PubMed  Google Scholar 

  • Polle E, Konzak CF, Kattrick JA (1978) Visual detection of aluminum tolerance levels in wheat by hematoxylin staining of seedling roots. Crop Sci 18:823–827

    Article  CAS  Google Scholar 

  • Poschenrieder C, Gunsé B, Corrales I, Barceló J (2008) A glance into aluminum toxicity and resistance in plants. Sci Total Environ 400:356–368

    Article  CAS  PubMed  Google Scholar 

  • Riaz M, Yan L, Wu X, Hussain S, Aziz O, Wang Y, Imran M, Jiang C (2017) Boron alleviates the aluminum toxicity in trifoliate orange by regulating antioxidant defense system and reducing root cell injury. J Environ Manag 208:149–158

    Article  Google Scholar 

  • Ruiz J, Rivero R, Romero L (2006) Boron increases synthesis of glutathione in sunflower plants subjected to aluminum stress. Plant Soil 279:25–30

    Article  CAS  Google Scholar 

  • Ryan P, Delhaize E, Randall P (1995) Malate efflux from root apices and tolerance to aluminium are highly correlated in wheat. Funct Plant Biol 22:531–536

    CAS  Google Scholar 

  • Tang N, Jiang H, Yang L, Li Q, Yang G, Chen L (2011) Boron-aluminum interactions affect organic acid metabolism more in leaves than in roots of Citrus grandis seedlings. Biol Plant 55:681–688

    Article  CAS  Google Scholar 

  • Vos C, Schat H, Waal M, Vooijs R, Ernst W (1991) Increased resistance to copper-induced damage of the root cell plasmalemma in copper tolerant Silene cucubalus. Physiol Plant 82:523–528

    Article  Google Scholar 

  • Wang F (1989) Theoretical single-ion activity coefficients in aqueous. J East China Inst Technol 51:46–52 (in Chinese with English abstract)

    Google Scholar 

  • Wang Z, Liu P (2013) Effect of citric acid inhibitor Mersal on antioxidant enzymes activities in oilseed rape leaves under aluminum stress. Jiangsu J Agric Sci 29:957–966 (in Chinese with English abstract)

    Google Scholar 

  • Wang F, Liu P, Xu G, Luo L (2005) Effects of aluminium on some physiological characters of buckwheat. J Agro-Environ Sci 24:678–681

    CAS  Google Scholar 

  • Xiao N, Tang H, Guo Q (1998) Study on sustainable development of rape production in China. Crops, pp 11–13 (in Chinese with English abstract)

  • Yan L, Jiang C, Muhammad R, Wu X, Lu X, Du C, Wang Y (2017) Mitigative effect of different forms of boron on aluminum toxicity of rape seedlings and its FTIR characteristics. Acta Agron Sin 43:1814–1823 (in Chinese with English abstract)

    Google Scholar 

  • Yang Y, Zhang H (1998) Boron amelioration of aluminum toxicity in mungbean seedlings. J Plant Nutr 21:1045–1054

    Article  CAS  Google Scholar 

  • Yang Y, Gu H, Fan W, Bilkisu A (2004) Effects of boron on aluminum toxicity on seedlings of two soybean cultivars. Water Air Soil Pollut 154:239–248

    Article  CAS  Google Scholar 

  • Yu M, Shen R, Xiao H (2009) Boron alleviates aluminum toxicity in pea. Plant Soil 314:87–98

    Article  CAS  Google Scholar 

  • Zhang F, Xu X (2001) Mitigative effect of exogenous boron on the wheat seedlings under aluminum stress. Plant Physiol Commun 37:21–24 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Zhang L, Wu J, Mei L, Wu J (2011) Saline tolerance of camptotheca acuminata provenances and the index selection for saline tolerance. Sci Silvae Sin 47:66–72

    Google Scholar 

  • Zhang H, Jiang Z, Wang C (2013) Effects of aluminum stress on soluble protein contents in roots and leaves of Hordeum vulgare L. Modern Agric Sci Technol 16:13–15

    Google Scholar 

Download references

Acknowledgements

The present work was supported by the “National Natural Science Foundation of China (41271320)” and the “Fundamental Research Funds for the Central Universities (2017PY055)”.

Author information

Authors and Affiliations

  1. Microelement Research Center, College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, Hubei, People’s Republic of China

    Lei Yan, Muhammad Riaz, Xiuwen Wu, Yuhan Wang, Chenqing Du & Cuncang Jiang

Authors
  1. Lei Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Muhammad Riaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiuwen Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuhan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chenqing Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cuncang Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cuncang Jiang.

Additional information

Communicated by S. Srivastava.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yan, L., Riaz, M., Wu, X. et al. Interaction of boron and aluminum on the physiological characteristics of rape (Brassica napus L.) seedlings. Acta Physiol Plant 40, 33 (2018). https://doi.org/10.1007/s11738-018-2614-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-018-2614-y

Keywords

Search

Navigation