Skip to main content
SpringerLink
Log in

Magnesium decreases aluminum accumulation and plays a role in protecting maize from aluminum-induced oxidative stress

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background

Acidic soils with a pHwater below 5.5 occupy up to 40% of world’s arable land. Aluminum (Al) toxicity and magnesium (Mg) deficiency often coexist in acidic soils, limiting crop production. In this study, we investigated a role of Mg in alleviation of Al stress in maize (Zea mays) by characterizing the growth responses, Al accumulation and the antioxidant properties of plants cultured hydroponically.

Methods

Physiological and molecular analyses were used to investigate the mechanisms of Mg governing the alleviation of Al-induced ROS production and root growth inhibition.

Results

Aluminum (50 μM) decreased root growth and induced oxidative stress. Exogenously added millimolar concentrations of Mg significantly alleviated Al toxicity as evidenced by restoration of plant growth, suppression of Al uptake, and a decline in root H2O2 concentration. Furthermore, the addition of Mg to the Al treatment solution enhanced the activities and expression of genes encoding superoxide dismutase, catalase and peroxidase compared to the Al-only treatment.

Conclusions

The results indicate that Mg plays a role in alleviation of Al toxicity, reduction of Al accumulation and protection from Al-induced oxidative stress through activation of antioxidative enzymes.

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

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

    CAS  PubMed  Google Scholar 

  • Awika J M (2011) Major cereal grains production and use around the world. pp. 1-13 in Cereal Science: Implications to Food Processing and Health Promotion, edited by Awika, J. M., V. Piironen, and S. Bean. American Chemical Society, Washington, DC.

  • Baligar VC, Schaffert RE, Dossantos HL, Pitta GVE, Filho AFDB (1993) Growth and nutrient-uptake parameters in sorghum as influenced by aluminum. Agron J 85:1068–1074. https://doi.org/10.2134/agronj1993.00021962008500050021x

    Article  CAS  Google Scholar 

  • Bose J, Babourina O, Rengel Z (2011) Role of magnesium in alleviation of aluminium toxicity in plants. J Exp Bot 62:2251–2264

    CAS  PubMed  Google Scholar 

  • Bose J, Babourina O, Shabala S, Rengel Z (2013) Low pH and aluminum resistance in Arabidopsis correlates with high cytosolic magnesium content and increased magnesium uptake by plant roots. Plant Cell Physiol 54:1093–1104

    CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Cakmak I, Kirkby EA (2008) Role of magnesium in carbon partitioning and alleviating photooxidative damage. Physiol Plant 133:692–704

    CAS  PubMed  Google Scholar 

  • Chen ZC, Ma JF (2013) Magnesium transporters and their role in Al tolerance in plants. Plant Soil 368(1–2):51–56

    CAS  Google Scholar 

  • Chen Q, Zhang X, Wang S, Wang Q, Wang G, Nian H, Li K, Yu Y, Chen L (2011) Transcriptional and physiological changes of alfalfa in response to aluminium stress. J Agric Sci 149:737–751

    CAS  Google Scholar 

  • Chen Q, Wu KH, Zhang YN, Phan XH, Li KZ, Yu YX, Chen LM (2012a) Physiological and molecular responses of broad bean (Vicia faba L.) to aluminum stress. Acta Physiol Plant 34:2251–2263

    CAS  Google Scholar 

  • Chen ZC, Yamaji N, Motoyama R, Nagamura Y, Ma JF (2012b) Up-regulation of a magnesium transporter gene OsMGT1 is required for conferring aluminum tolerance in rice. Plant Physiol 159:1624–1633

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Q, Kan Q, Wang P, Yu W, Yu Y, Zhao Y, Yu Y, Li K, Chen L (2015) Phosphorylation and interaction with the 14-3-3 protein of the plasma membrane H+-ATPase are involved in the regulation of magnesium-mediated increases in aluminum-induced citrate exudation in broad bean (Vicia faba. L), Plant Cell Physiol 56(6):1144–1153

  • Cristancho RJA, Hanafi MM, Syed OSR, Rafii MY (2014) Aluminium speciation of amended acid tropical soil and its effects on plant root growth. J Plant Nutr 37(6):811–827. https://doi.org/10.1080/01904167.2014.881856

  • Darkó É, Ambrusa H, Stefanovits-Bányaib É, Fodorc J, Bakosa F, Barnabása B (2004) Aluminium toxicity, Al tolerance and oxidative stress in an Al-sensitive wheat genotype and in Al-tolerant lines developed by in vitro microspore selection. Plant Sci 166:583–591

    Google Scholar 

  • Deng W, Luo K, Li D, Zheng X, Wei X, Smith W, Thammina C, Lu L, Li Y, Pei Y (2006) Overexpression of an Arabidopsis magnesium transport gene, AtMGT1, in Nicotiana benthamiana confers Al tolerance. J Exp Bot 57:4235–4243

  • Ezaki B, Gardner RC, Ezaki Y, Matsumoto H (2000) Expression of aluminum-induced genes in transgenic arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol 122:657–665

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo W, Nazim H, Liang Z, Yang D (2016) Magnesium deficiency in plants: An urgent problem. Crop Journal 4(2): 83-91Guo W, Nazim H, Liang Z, Yang D (2016). Magnesium deficiency in plants: An urgent problem. Crop Journal 4(2):83–91

  • Giannakoula A, Moustakas M, Mylona P, Papadakis I, Yupsanis T (2008) Aluminum tolerance in maize is correlated with increased levels of mineral nutrients, carbohydrates and proline, and decreased levels of lipid peroxidation and Al accumulation. J Plant Physiol 165:385–396

    CAS  PubMed  Google Scholar 

  • Giannakoula A, Moustakas M, Syros T, Yupsanis T (2010) Aluminum stress induces up-regulation of an efficient antioxidant system in the Al-tolerant maize line but not in the Al-sensitive line. Environ Exp Bot 67(3):487–494

    CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Iuchi S, Koyama H, Iuchi A, Kobayashi Y, Kitabayashi S, Kobayashi Y, Ikka T, Hirayama T, Shinozaki K, Kobayashi M (2007) Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc Natl Acad Sci USA 104(23):9900–9905

    PubMed  PubMed Central  Google Scholar 

  • Kasongo RK, Ranst EV, Kanyankogote P, Verdoodt A, Baert G (2012) Response of soybean (Glycine max ) to Kanzi rock phosphate and Kimpese pink dolomite application on a sandy soil in DR Congo. Can J Soil Sci 92:905–916

    CAS  Google Scholar 

  • Knoop V, Groth-Malonek M, Gebert M, Eifler K, Weyand K (2005) Transport of magnesium and other divalent cations: evolution of the 2-TM-GxN proteins in the MIT superfamily. Mol Gen Genomics 274(3):205–216

    CAS  Google Scholar 

  • Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493

    CAS  PubMed  Google Scholar 

  • Li L, Tutone AF, Drummond RS, Gardner RC, Luan S (2001) A novel family of magnesium transport genes in Arabidopsis. Plant Cell 13(12):2761–2775

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Du H, Huang K et al (2016) Identification, and functional and expression analyses of the CorA/MRS2/MGT-type magnesium transporter family in maize. Plant Cell Physiol 57(6):1153–1168

    CAS  PubMed  Google Scholar 

  • Li D, Ma W, Wei J, Mao Y, Peng Z, Zhang J, Kong X, Han Q, Fan W, Yang Y, Chen J, Wu L, Rengel Z, Cui X, Chen Q (2019) Magnesium promotes root growth and increases aluminum tolerance via modulation of nitric oxide production in Arabidopsis. Plant Soil. https://doi.org/10.1007/s11104-019-04274-9

  • Ma JF, Chen ZC, Shen RF (2014) Molecular mechanisms of Al tolerance in gramineous plants. Plant Soil 381(1–2):1–12

    CAS  Google Scholar 

  • Maehly AC, Chance B (1954) The assay of catalases and peroxidases. Methods Biochem Anal 1:357–424

    CAS  PubMed  Google Scholar 

  • Mao DD, Chen J, Tian LF, Liu Z, Yang L, Tang R, Li J, Lu CQ, Yang YH, Shi JS, Chen LB, Li DP, Luan S (2014) Arabidopsis transporter MGT6 mediates magnesium uptake and is required for growth under magnesium limitation. Plant Cell 26:2234–2248

  • Mariano ED, Keltjens WG (2005) Long-term effects of aluminum exposure on nutrient uptake by maize genotypes differing in aluminum resistance. J Plant Nutr 28:323–333

    CAS  Google Scholar 

  • Maschietto V, Lanubile A, Leonardis SD (2016) Constitutive expression of pathogenesis-related proteins and antioxydant enzyme activities triggers maize resistance towards Fusarium verticillioides. J Plant Physiol 200:53–61

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Pandey P, Srivastava RK, Dubey RS (2013) Salicylic acid alleviates aluminum toxicity in rice seedlings better than magnesium and calcium by reducing aluminum uptake, suppressing oxidative damage and increasing antioxidative defense. Ecotoxicology 22(4):656–670

    CAS  PubMed  Google Scholar 

  • Pérez V, Wherrett T, Shabala S, Muniz J, Dobrovinskaya O, Pottosin I (2008) Homeostatic control of slow vacuolar channels by luminal cations and evaluation of the channel-mediated tonoplast Ca2+ fluxes in situ. J Exp Bot 59(14):3845–3855

    PubMed  PubMed Central  Google Scholar 

  • Rengel Z, Zhang WH (2003) Role of dynamics of intracellular calcium in aluminium toxicity syndrome. New Phytol 159:295–314

    CAS  PubMed  Google Scholar 

  • Rengel Z, Bose J, Chen Q, Tripathi BN (2015) Magnesium alleviates plant toxicity of aluminium and heavy metals. Crop Pasture Sci 66:1298–1307

    CAS  Google Scholar 

  • Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116:409–418

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ryan PR, Reid RJ, Smith FA (1997) Direct evaluation of the Ca2+-displacement hypothesis for Al toxicity. Plant Physiol 113:1351–1357

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saito T, Kobayashi NI, Tanoi K, Iwata N, Suzuki H, Iwata R, Nakanishi TM (2013) Expression and functional analysis of the CorA-MRS2-ALR-type magnesium transporter family in rice. Plant Cell Physiol 54(10):1673–1683

    CAS  PubMed  Google Scholar 

  • Schock I, Gregan J, Steinhauser S, Schweyen R, Brennicke A, Knoop V (2000) A member of a novel Arabidopsis thaliana gene family of candidate Mg2+ ion transporters complements a yeast mitochondrial group II intron-splicing mutant. Plant J 24(4):489–501

    CAS  PubMed  Google Scholar 

  • Shi F, Zhang Y, Wang K, Meng Q, Liu X, Ma L, Li Y, Liu J, Ma L (2018) Expression profile analysis of maize in response to Setosphaeria turcica. Gene 659:100–108

    CAS  PubMed  Google Scholar 

  • Silva IR, Smyth TJ, Israel DW, Raper CD, Rufty TW (2001) Magnesium ameliorates aluminum rhizotoxicity in soybean by increasing citric acid production and exudation by roots. Plant Cell Physiol 42:546–554

    CAS  PubMed  Google Scholar 

  • Silva S, Pinto-Carnide O, Martins-Lopes P, Matos M, Guedes-Pinto H, Santos C (2010) Differential aluminium changes on nutrient accumulation and root differentiation in an Al sensitive vs. tolerant wheat. Environ Exp Bot 68:91–98

    CAS  Google Scholar 

  • Sivaguru M, Paliwal K (1993) Differential aluminum tolerance in some tropical rice cultivars. 2. Mechanism of aluminum tolerance. J Plant Nutr 16:1717–1732

    CAS  Google Scholar 

  • Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923

    CAS  PubMed  Google Scholar 

  • Wang YS, Wang J, Yang ZM, Wang QY, Lu B, Li SQ, Lu YP, Wang SH, Sun X (2004) Salicylic acid modulates aluminum-induced oxidative stress in roots of Cassia tora. Acat Bot Sin 46:819–828. http://www.chineseplantscience.com

    CAS  Google Scholar 

  • Watanabe T, Okada K (2005) Interactive effects of Al, Ca and other cations on root elongation of rice cultivars under low pH. Ann Bot 95:379–385

    CAS  PubMed  Google Scholar 

  • Wherrett T, Shabala S, Pottosin I (2005) Different properties of SV channels in root vacuoles from near isogenic Al-tolerant and Al-sensitive wheat cultivars. FEBS Lett 579(30):6890–6894

    CAS  PubMed  Google Scholar 

  • White PJ, Broadley MR, El-Serehy HA, George TS, NeugebauerK (2018) Linear relationships between shoot magnesium and calcium concentrations among angiosperm species are associated with cell wall chemistry. Ann Bot 122(2):221–226

    CAS  PubMed  PubMed Central  Google Scholar 

  • Whitten MG, Wong MTF, Rate AW (2000) Amelioration of subsurface acidity in the south-west of Western Australia: downward movement and mass balance of surface-incorporated lime after 2-15 years. Aust J Soil Res 38:711–728

    Google Scholar 

  • Wu Y, Yang Z, How J, Xu H, Chen L, Li K (2017) Overexpression of a peroxidase gene (AtPrx64) of Arabidopsis thaliana in tobacco improves plant’s tolerance to aluminum stress. Plant Mol Biol 95(1–2):157–168

    CAS  PubMed  Google Scholar 

  • Yang JL, You JF, Li YY, Wu P, Zheng SJ (2007) Magnesium enhances aluminum-induced citrate secretion in rice bean roots (Vigna umbellata) by restoring plasma membrane H+-ATPase activity. Plant Cell Physiol 48:66–73

    CAS  PubMed  Google Scholar 

  • Yang ZB, Geng X, He C, Zhang F, Wang R, Horst WJ, Ding Z (2014) TAA1-regulated local auxin biosynthesis in the root-apex transition zone mediates the aluminum-induced inhibition of root growth in Arabidopsis. Plant Cell 26(7):2889–2904

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yi HL, Yi M, Li HH, Wu LH (2010) Aluminum induces chromosome aberrations, micronuclei, and cell cycle dysfunction in root cells of Vicia faba. Environ Toxicol 25:124–129

    CAS  PubMed  Google Scholar 

  • Yoko Y, Yukiko K, Hideaki M (2001) Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125:199–208. https://doi.org/10.1104/pp.125.1.199

    Article  Google Scholar 

  • Zhang J, Zeng B, Mao Y, Kong X, Xu J, Rengel Z, Chen Q (2017) Melatonin alleviates aluminium toxicity through modulating antioxidative enzymes and enhancing organic acid anion exudation in soybean. Funct Plant Biol 44:961–968

    CAS  PubMed  Google Scholar 

  • Zhang L, Peng Y, Li J, Tian X, Chen Z (2019) OsMGT1 confers resistance to magnesium deficiency by enhancing the import of Mg in rice. Int J Mol Sci 20:207

    PubMed Central  Google Scholar 

  • Zheng SJ (2010) Crop production on acidic soils: overcoming aluminium toxicity and phosphorus deficiency. Ann Bot 106:183–184

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 31960624, 31660595, 31501832 and 31360340), Science and Technology Project of Yunnan province (2017FB063), and Natural Science Foundation of Guangdong province (2018A030310192). Zed Rengel was supported by Australian Research Council (DP160104434).

Author information

Author notes

  1. Xiangying Kong and Zhongping Peng contributed equally to this work.

Authors and Affiliations

  1. Faculty of Life Science and Technology, Kunming University of Science and Technology, Jingming South Road, Kunming, 650500, China

    Xiangying Kong, Zhongping Peng, Dongxu Li, Wenna Ma, Ruidong An, Dawood Khan, Yuan Liu, En Yang & Qi Chen

  2. Faculty of Architecture and City Planning, Kunming University of Science and Technology, Jingming South Road, Kunming, 650500, China

    Xiangying Kong

  3. UWA School of Agriculture and Environment, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Perth, WA, 6009, Australia

    Xinxun Wang, Zed Rengel & Qi Chen

  4. Vegetable Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, 501640, China

    Yuzhi He & Baige Zhang

  5. International Magnesium Institute, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Liqngquan Wu

  6. Institute for Adriatic Crops and Karst reclamation, Put Duilova 11, 21000, Split, Croatia

    Zed Rengel

  7. Yunnan Rural Science and Technology Service Center, Kunming, 650021, China

    Jianmin Wang

Authors
  1. Xiangying Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhongping Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dongxu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wenna Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ruidong An
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dawood Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xinxun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yuan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. En Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yuzhi He
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Liqngquan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Baige Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Zed Rengel
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Jianmin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Qi Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Baige Zhang or Qi Chen.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Responsible Editor: Ismail Cakmak.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kong, X., Peng, Z., Li, D. et al. Magnesium decreases aluminum accumulation and plays a role in protecting maize from aluminum-induced oxidative stress. Plant Soil 457, 71–81 (2020). https://doi.org/10.1007/s11104-020-04605-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-020-04605-1

Keywords

Search

Navigation