Up-Regulation of a Magnesium Transporter Gene OsMGT1 Is Required for Conferring Aluminum Tolerance in Rice1[W][OA]

Magnesium (Mg)-mediated alleviation of aluminum (Al) toxicity has been observed in a number of plant species, but the mechanisms underlying the alleviation are still poorly understood. When a putative rice (Oryza sativa) Mg transporter gene, Oryza sativa MAGNESIUM TRANSPORTER1 (OsMGT1), was knocked out, the tolerance to Al, but not to cadmium and lanthanum, was decreased. However, this inhibition could be rescued by addition of 10 μm Mg, but not by the same concentration of barium or strontium. OsMGT1 was expressed in both the roots and shoots in the absence of Al, but the expression only in the roots was rapidly up-regulated by Al. Furthermore, the expression did not respond to low pH and other metals including cadmium and lanthanum, and was regulated by an Al-responsive transcription factor, AL RESISTANCE TRANSCRIPTION FACTOR1. An investigation of subcellular localization showed that OsMGT1 was localized to the plasma membrane. A short-term (30 min) uptake experiment with stable isotope 25Mg showed that knockout of OsMGT1 resulted in decreased Mg uptake, but that the uptake in the wild type was enhanced by Al. Mg concentration in the cell sap of the root tips was also increased in the wild-type rice, but not in the knockout lines in the presence of Al. A microarray analysis showed that transcripts of genes related to stress were more up- and down-regulated in the knockout lines. Taken together, our results indicate that OsMGT1 is a transporter for Mg uptake in the roots and that up-regulation of this gene is required for conferring Al tolerance in rice by increasing Mg concentration in the cell.

[1]  E. Delhaize,et al.  Transcriptional regulation of aluminium tolerance genes. , 2012, Trends in plant science.

[2]  Chao-Feng Huang,et al.  A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. , 2012, The Plant journal : for cell and molecular biology.

[3]  N. Yamaji,et al.  An Al-inducible MATE gene is involved in external detoxification of Al in rice. , 2011, The Plant journal : for cell and molecular biology.

[4]  Keyan Zhao,et al.  Genetic Architecture of Aluminum Tolerance in Rice (Oryza sativa) Determined through Genome-Wide Association Analysis and QTL Mapping , 2011, PLoS genetics.

[5]  Y. Chao,et al.  Effect of potassium deficiency on antioxidant status and cadmium toxicity in rice seedlings , 2011, Botanical Studies.

[6]  B. Waters Moving magnesium in plant cells. , 2011, The New phytologist.

[7]  T. Nakanishi,et al.  The analysis of magnesium transport system from external solution to xylem in rice root , 2011 .

[8]  Z. Rengel,et al.  Role of magnesium in alleviation of aluminium toxicity in plants. , 2011, Journal of experimental botany.

[9]  Dabing Zhang,et al.  Rice MADS3 Regulates ROS Homeostasis during Late Anther Development[W][OA] , 2011, Plant Cell.

[10]  K. Török,et al.  Overproduction of a rice aldo–keto reductase increases oxidative and heat stress tolerance by malondialdehyde and methylglyoxal detoxification , 2011, Plant Molecular Biology.

[11]  N. Yamaji,et al.  Plasma membrane-localized transporter for aluminum in rice , 2010, Proceedings of the National Academy of Sciences.

[12]  K. Solimán,et al.  Mechanisms of magnesium amelioration of aluminum toxicity in soybean at the gene expression level. , 2010, Genome.

[13]  Julian Weghuber,et al.  A Root-Expressed Magnesium Transporter of the MRS2/MGT Gene Family in Arabidopsis thaliana Allows for Growth in Low-Mg2+ Environments[W] , 2009, The Plant Cell Online.

[14]  M. Yano,et al.  A Zinc Finger Transcription Factor ART1 Regulates Multiple Genes Implicated in Aluminum Tolerance in Rice[C][W] , 2009, The Plant Cell Online.

[15]  Liang-bi Chen,et al.  Magnesium transporter AtMGT9 is essential for pollen development in Arabidopsis , 2009, Cell Research.

[16]  N. Sakurai,et al.  STOP1 Regulates Multiple Genes That Protect Arabidopsis from Proton and Aluminum Toxicities1[C][W][OA] , 2009, Plant Physiology.

[17]  M. Yano,et al.  A Bacterial-Type ABC Transporter Is Involved in Aluminum Tolerance in Rice[W] , 2009, The Plant Cell Online.

[18]  N. Sakurai,et al.  STOP 1 Regulates Multiple Genes That Protect Arabidopsis from Proton and Aluminum Toxicities 1 [ C ] [ W ] [ OA ] , 2009 .

[19]  N. Sakurai,et al.  Comparative transcriptomic characterization of aluminum, sodium chloride, cadmium and copper rhizotoxicities in Arabidopsis thaliana , 2009, BMC Plant Biology.

[20]  S. Luan,et al.  AtMGT7: An Arabidopsis gene encoding a low-affinity magnesium transporter. , 2008, Journal of integrative plant biology.

[21]  M. Maguire,et al.  The unique nature of mg2+ channels. , 2008, Physiology.

[22]  E. A. Kirkby,et al.  Role of magnesium in carbon partitioning and alleviating photooxidative damage. , 2008, Physiologia plantarum.

[23]  S. Luan,et al.  A mitochondrial magnesium transporter functions in Arabidopsis pollen development. , 2008, Molecular plant.

[24]  M. Maguire,et al.  The Unique Nature of Mg 2 + Channels , 2008 .

[25]  Pallavi Sharma,et al.  Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum , 2007, Plant Cell Reports.

[26]  S. Zheng,et al.  Magnesium enhances aluminum-induced citrate secretion in rice bean roots (Vigna umbellata) by restoring plasma membrane H+-ATPase activity. , 2007, Plant & cell physiology.

[27]  N. Yamaji,et al.  Spatial Distribution and Temporal Variation of the Rice Silicon Transporter Lsi1 , 2007 .

[28]  J. Ma,et al.  Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. , 2007, International review of cytology.

[29]  Demou Li,et al.  Overexpression of an Arabidopsis magnesium transport gene, AtMGT1, in Nicotiana benthamiana confers Al tolerance. , 2006, Journal of experimental botany.

[30]  Kenji Umemura,et al.  A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice. , 2006, Molecular plant pathology.

[31]  W. G. Keltjens,et al.  Role of magnesium in combination with liming in alleviating acid-soil stress with the aluminium-sensitive sorghum genotype CV323 , 1991, Plant and Soil.

[32]  R. Gardner,et al.  A putative magnesium transporter AtMRS2-11 is localized to the plant chloroplast envelope membrane system , 2006 .

[33]  Michael Gebert,et al.  Transport of magnesium and other divalent cations: evolution of the 2-TM-GxN proteins in the MIT superfamily , 2005, Molecular Genetics and Genomics.

[34]  Toshihiro Watanabe,et al.  Interactive effects of Al, Ca and other cations on root elongation of rice cultivars under low pH. , 2005, Annals of botany.

[35]  L. Kochian,et al.  How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. , 2004, Annual review of plant biology.

[36]  N. Soranzo,et al.  Organisation and structural evolution of the rice glutathione S-transferase gene family , 2004, Molecular Genetics and Genomics.

[37]  D. Parker,et al.  Relative effectiveness of calcium and magnesium in the alleviation of rhizotoxicity in wheat induced by copper, zinc, aluminum, sodium, and low pH , 2004, Plant and Soil.

[38]  T. Rufty,et al.  Altered aluminum inhibition of soybean root elongation in the presence of magnesium , 2001, Plant and Soil.

[39]  L. Kochian,et al.  Al3+-Ca2+ interactions in aluminum rhizotoxicity , 1993, Planta.

[40]  L. Kochian,et al.  Al3+-Ca2+ interactions in aluminum rhizotoxicity , 1993, Planta.

[41]  B. K. Reddy,et al.  Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). , 2004, Journal of plant physiology.

[42]  T. Kinraide Toxicity factors in acidic forest soils: attempts to evaluate separately the toxic effects of excessive Al3+ and H+ and insufficient Ca2+ and Mg2+ upon root elongation , 2003 .

[43]  T. Vision,et al.  Identification and Characterization of Aluminum Tolerance Loci in Arabidopsis (Landsberg erecta × Columbia) by Quantitative Trait Locus Mapping. A Physiologically Simple But Genetically Complex Trait1 , 2003, Plant Physiology.

[44]  Yoshinobu Takeuchi,et al.  Response of rice to Al stress and identification of quantitative trait Loci for Al tolerance. , 2002, Plant & cell physiology.

[45]  S. Luan,et al.  A Novel Family of Magnesium Transport Genes in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010352. , 2001, The Plant Cell Online.

[46]  T. Rufty,et al.  Magnesium ameliorates aluminum rhizotoxicity in soybean by increasing citric acid production and exudation by roots. , 2001, Plant & cell physiology.

[47]  A. Brennicke,et al.  A member of a novel Arabidopsis thaliana gene family of candidate Mg2+ ion transporters complements a yeast mitochondrial group II intron-splicing mutant. , 2000, The Plant journal : for cell and molecular biology.

[48]  J. F. Ma,et al.  Role of organic acids in detoxification of aluminum in higher plants. , 2000, Plant & cell physiology.

[49]  R. Gardner,et al.  Overexpression of the Saccharomyces cerevisiaeMagnesium Transport System Confers Resistance to Aluminum Ion* , 1998, The Journal of Biological Chemistry.

[50]  D. Mount,et al.  Evidence That Heat and Ultraviolet Radiation Activate a Common Stress-Response Program in Plants That Is Alterd in the uvh6 Mutant of Arabidopsis thaliana , 1997, Plant physiology.

[51]  F. A. Smith,et al.  Direct Evaluation of the Ca2+-Displacement Hypothesis for Al Toxicity , 1997, Plant physiology.

[52]  C. Fierke,et al.  Magnesium ions are required by Bacillus subtilis ribonuclease P RNA for both binding and cleaving precursor tRNAAsp. , 1996, Biochemistry.

[53]  T. Kiss,et al.  The bioinorganic chemistry of aluminum , 1996 .

[54]  R. Crouch,et al.  The non-RNase H domain of Saccharomyces cerevisiae RNase H1 binds double-stranded RNA: magnesium modulates the switch between double-stranded RNA binding and RNase H activity. , 1995, RNA.

[55]  T. Rufty,et al.  Rapid Uptake of Aluminum into Cells of Intact Soybean Root Tips (A Microanalytical Study Using Secondary Ion Mass Spectrometry) , 1994, Plant physiology.

[56]  E. Delhaize,et al.  Aluminum Tolerance in Wheat (Triticum aestivum L.) (II. Aluminum-Stimulated Excretion of Malic Acid from Root Apices) , 1993, Plant physiology.

[57]  N. Pace,et al.  Multiple magnesium ions in the ribonuclease P reaction mechanism. , 1993, Biochemistry.

[58]  W. Horst,et al.  Modeling Cation Amelioration of Aluminum Phytotoxicity , 1992 .

[59]  W. G. Keltjens,et al.  Aluminium toxicity with sorghum genotypes in nutrient solutions and its amelioration by magnesium. , 1992 .

[60]  D. L. Robinson,et al.  Aluminum Effects on Growth and Macronutrient Uptake by Annual Ryegrass , 1989 .

[61]  A. Noble,et al.  Calcium and Al interactions and soybean growth in nutrient solutions , 1988 .

[62]  E. Epstein Mineral Nutrition of Plants: Principles and Perspectives , 1972 .