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.
Physiological and molecular analyses were used to investigate the mechanisms of Mg governing the alleviation of Al-induced ROS production and root growth inhibition.
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.
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 to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
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
Bose J, Babourina O, Rengel Z (2011) Role of magnesium in alleviation of aluminium toxicity in plants. J Exp Bot 62:2251–2264
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
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
Cakmak I, Kirkby EA (2008) Role of magnesium in carbon partitioning and alleviating photooxidative damage. Physiol Plant 133:692–704
Chen ZC, Ma JF (2013) Magnesium transporters and their role in Al tolerance in plants. Plant Soil 368(1–2):51–56
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
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
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
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
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
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
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
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
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314
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
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
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
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
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
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
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
Maehly AC, Chance B (1954) The assay of catalases and peroxidases. Methods Biochem Anal 1:357–424
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
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
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
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
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
Rengel Z, Zhang WH (2003) Role of dynamics of intracellular calcium in aluminium toxicity syndrome. New Phytol 159:295–314
Rengel Z, Bose J, Chen Q, Tripathi BN (2015) Magnesium alleviates plant toxicity of aluminium and heavy metals. Crop Pasture Sci 66:1298–1307
Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116:409–418
Ryan PR, Reid RJ, Smith FA (1997) Direct evaluation of the Ca2+-displacement hypothesis for Al toxicity. Plant Physiol 113:1351–1357
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
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
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
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
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
Sivaguru M, Paliwal K (1993) Differential aluminum tolerance in some tropical rice cultivars. 2. Mechanism of aluminum tolerance. J Plant Nutr 16:1717–1732
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
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
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
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
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
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
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
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
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
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
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
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
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
Zheng SJ (2010) Crop production on acidic soils: overcoming aluminium toxicity and phosphorus deficiency. Ann Bot 106:183–184
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).
Conflict of interest
The authors declare no conflicts of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Responsible Editor: Ismail Cakmak.
About this article
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 (2020). https://doi.org/10.1007/s11104-020-04605-1
- Al toxicity
- Antioxidative enzymes