Abstract
Key message
ZmMGT10 was specifically expressed in maize roots and induced by a deficiency of magnesium. Overexpression of ZmMGT10 restored growth deficiency of the Salmonella typhimurium MM281 strain and enhanced the tolerance in Arabidopsis to stress induced by low magnesium levels by increasing uptake of Mg2+ via roots.
Abstract
CorA/MRS2/MGT-type Mg2+ transporters play a significant role in maintaining magnesium (Mg) homeostasis in plants. Although the maize CorA/MRS2/MGT family comprises of 12 members, currently no member has been functionally characterized. Here, we report the isolation and functional characterization of ZmMGT10 from the maize MRS2/MGT gene family. ZmMGT10 has a typical structure feature which includes two conserved TMs near the C-terminal end and an altered AMN tripeptide motif. The high sequence similarity and close phylogenetic relationship indicates that ZmMGT10 is probably the counterpart of Arabidopsis AtMGT6. The complementation of the Salmonella typhimurium mutated MM281 strain indicates that ZmMGT10 possesses the ability to transport Mg2+. ZmMGT10 was specifically expressed in the plant roots and it can be stimulated by a deficiency of Mg. Transgenic Arabidopsis plants which overexpressed ZmMGT10 grew more vigorously than wild-type plants under low Mg conditions, exhibited by longer root length, higher plant fresh weight and chlorophyll content, suggesting ZmMGT10 was essential for plant growth and development under low Mg conditions. Further investigations found that high accumulation of Mg2+ occurred in transgenic plants attributed to improved Mg2+ uptake and thereby enhanced tolerance to Mg deficiency. Results from this investigation illustrate that ZmMGT10 is a Mg transporter of maize which can enhance the tolerance to Mg deficient conditions by improving Mg2+ uptake in the transgenic plants of Arabidopsis.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Brady KU, Kruckeberg AR, Bradshaw HD Jr (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266
Cakmak I, Yazici AM (2010) Magnesium: a forgotten element in crop production Better Crops Plant Food 94:23–25
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium -mediated transformation of Arabidopsis thaliana. Plant J Cell Mol Biol 16:735
Conn SJ, Conn V, Tyerman SD, Kaiser BN, Leigh RA, Gilliham M (2011) Magnesium transporters, MGT2/MRS2-1 and MGT3/MRS2-5, are important for magnesium partitioning within Arabidopsis thaliana mesophyll vacuoles. New Phytol 190:583–594
Coppens F (2010) Systems analysis of the responses to long-term magnesium deficiency and restoration in Arabidopsis thaliana. New Phytol 187:132
Deng W et al (2006) Overexpression of an Arabidopsis magnesium transport gene, AtMGT1, in Nicotiana benthamiana confers Al tolerance. J Exp Bot 57:4235–4243
Drummond RSM, Tutone A, Li YC, Gardner RC (2006) A putative magnesium transporter AtMRS2-11 is localized to the plant chloroplast envelope membrane system. Plant Sci 170:78–89
Gebert M, Meschenmoser K, Svidová S, Weghuber J, Schweyen R, Eifler K, Lenz H, Weyand K, Knoop V (2009) A root-expressed magnesium transporter of the MRS2/MGT gene family in Arabidopsis thaliana allows for growth in low-Mg2+ environments. Plant Cell 21:4018–4030
Georges B, Emile K, Alexandra P, Andrée H, Laurent C, Pierre T, Claire P (2003) A novel high efficiency, low maintenance, hydroponic system for synchronous growth and flowering of Arabidopsis thaliana. BMC Plant Biol 3:2
Gransee A, Führs H (2013) Magnesium mobility in soils as a challenge for soil and plant analysis, magnesium fertilization and root uptake under adverse growth conditions. Plant Soil 368:5–21
Grbic V, Bleecker AB (2003) Ethylene regulates the timing of leaf senescence in Arabidopsis. Plant J 8:595–602
Gu R, Chen X, Zhou Y, Yuan L (2012) Isolation and characterization of three maize aquaporin genes, ZmNIP2;1, ZmNIP2;4 and ZmTIP4;4 involved in urea transport. BMB Rep 45:96–101
Guo W et al (2014) The remodeling of seedling development in response to long-term magnesium toxicity and regulation by ABA-DELLA signaling in Arabidopsis. Plant Cell Physiol 55:1713–1726
Guo W, Nazim H, Liang Z, Yang D (2016) Magnesium deficiency in plants: an urgent problem. Crop J 4:83–91
Hermans C, Vuylsteke M, Coppens F, Craciun A, Inzé D, Verbruggen N (2010) Early transcriptomic changes induced by magnesium deficiency in Arabidopsis thaliana reveal the alteration of circadian clock gene expression in roots and the triggering of abscisic acid-responsive genes. New Phytol 187:119–131
Hörtensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14:155
Knoop V et al (2005) Transport of magnesium and other divalent cations: evolution of the 2-TM-GxN proteins in the MIT superfamily. Mol Genet Genom 274:205
Kobayashi NI, Saito T, Iwata N, Ohmae Y, Iwata R, Tanoi K, Nakanishi TM (2012) Leaf senescence in rice due to magnesium deficiency-mediated defect in transpiration rate before sugar accumulation and chlorosis. Physiol Plant 148:490–501
Krogh A, Larsson B, Von HG, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567
Leggett JE (1969) Magnesium uptake by soybeans. Plant Physiol 44:1182–1186
Li L, Tutone AF, Drummond RS, Gardner RC, Luan S (2001) A novel family of magnesium transport genes in Arabidopsis. Plant Cell 13:2761–2775
Li L-G et al. (2008) A mitochondrial magnesium transporter functions in Arabidopsis pollen development. Mol Plant 1:675–685
Li H et al (2016) Identification, and functional and expression analyses of the CorA/MRS2/MGT-type magnesium transporter family in maize. Plant Cell Physiol 57:1153
Maas EV, Ogata G (1971) Absorption of magnesium and chloride by excised corn root. Plant Physiol 47:357
Mao D et al (2014) Arabidopsis transporter MGT6 mediates magnesium uptake and is required for growth under magnesium limitation. Plant Cell 26:2234
Molinerorosales N, Latorre A, Jamilena M, Lozano R (2004) SINGLE FLOWER TRUSS regulates the transition and maintenance of flowering in tomato. Planta 218:427–434
Oda K, Kamiya T, Shikanai Y, Shigenobu S, Yamaguchi K, Fujiwara T (2016) The Arabidopsis Mg transporter, MRS2-4, is essential for Mg homeostasis under both low and high Mg conditions. Plant Cell Physiol 57:754–763
Rengel Z, Robinson DL (1990) Competitive Al3+ inhibition of net Mg2+ uptake by intact Lolium multiflorum roots: I. Kinetics. Plant Physiol 93:1261–1267
Saitou N, Nei M (1987) The neighbor-joining method-a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425
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 24:489–501
Shaul O (2002) Magnesium transport and function in plants: the tip of the iceberg. Biometals 15:309
Szegedy MA, Maguire ME (1999) The CorA Mg(2+) transport protein of Salmonella typhimurium. Mutagenesis of conserved residues in the second membrane domain. J Biol Chem 274:36973–36979
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tanoi K, Saito T, Iwata N, Kobayashi NI, Nakanishi TM (2011) The analysis of magnesium transport system from external solution to xylem in rice root. Soil Sci Plant Nutr 57:265–271
Tanoi K et al (2014) Effects of magnesium deficiency on magnesium uptake activity of rice root, evaluated using 28 Mg as a tracer. Plant Soil 384:69–77
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Verbruggen N, Hermans C (2013) Physiological and molecular responses to magnesium nutritional imbalance in plants. Plant Soil 368:87–99
Wilkinson SR, Welch RM, Mayland HF, Grunes DL (1990) Magnesium in plants: uptake, distribution, function and utilization by man and animals. Met Ions Biol Syst 26:33–56
Williams L, Salt DE (2009) The plant ionome coming into focus. Curr Opin Plant Biol 12:247–249
Zhi CC, Jian FM (2012) Up-regulation of a magnesium transporter gene OsMGT1 is required for conferring aluminum tolerance in rice. Plant Physiol 159:1624–1633
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Nos. 30800687, 31071434), Major Project of Education Department in Sichuan (No.15ZA0022). The authors are very grateful to Professor Legong Li (College of Life Sciences, Capital Normal University, China) for providing S. typhimurium strain MM281 and plasmid pTrc99A.
Author information
Authors and Affiliations
Contributions
HL carried out the experiments, data analysis and drafted the manuscript. NW carried out partial experiments. JD, HD, KH, contributed to sample collection. MC, YL, SG, and TR contributed to consultation, SZ managed and designed the experiment and prepared the manuscript.
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Li, H., Wang, N., Ding, J. et al. The maize CorA/MRS2/MGT-type Mg transporter, ZmMGT10, responses to magnesium deficiency and confers low magnesium tolerance in transgenic Arabidopsis . Plant Mol Biol 95, 269–278 (2017). https://doi.org/10.1007/s11103-017-0645-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-017-0645-1