Expression and functional analysis of the CorA-MRS2-ALR-type magnesium transporter family in rice

Plant and Cell Physiology

Volumn 54, Issue 10, 2013, Pages 1673-1683

  Saito, Takayuki ^a   Kobayashi, Natsuko I ^a   Tanoi, Keitaro ^a   Iwata, Naoko ^a   Suzuki, Hisashi ^b   Iwata, Ren ^c   Nakanishi, Tomoko M ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^c TOHOKU UNIVERSITY   (Japan)

Author keywords

28Mg; Chloroplast; CorA; Magnesium; MRS2 MGT; Oryza sativa

Indexed keywords

CATION TRANSPORT PROTEIN; GREEN FLUORESCENT PROTEIN; ISOPROTEIN; MAGNESIUM; VEGETABLE PROTEIN;

28MG; AMINO ACID SEQUENCE; ARTICLE; CHLOROPLAST; CLASSIFICATION; CONFOCAL MICROSCOPY; CORA; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MRS2/MGT; MULTIGENE FAMILY; MUTATION; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTOPLAST; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RICE; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; TIME;

28MG; CHLOROPLAST; CORA; MAGNESIUM; MRS2/MGT; ORYZA SATIVA;

AMINO ACID SEQUENCE; BASE SEQUENCE; CATION TRANSPORT PROTEINS; CHLOROPLASTS; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; GREEN FLUORESCENT PROTEINS; MAGNESIUM; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTATION; ORYZA SATIVA; PHYLOGENY; PLANT PROTEINS; PROTEIN ISOFORMS; PROTOPLASTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; TIME FACTORS;

EID: 84885901762     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pct112     Document Type: Article

References (38)

1. Bui, D.M., Gregan, J., Jarosch, E., Ragnini, A. and Schweyen, R.J. (1999) The bacterial magnesium transporter CorA can functionally substitute for its putative homologue Mrs2p in the yeast inner mitochondrial membrane. J. Biol. Chem. 274: 20438-20443.
2. Chen, A.C., Yamaji, N., Motoyama, R., Nagamura, Y. and Ma, J.F. (2012) Up-regulation of a magnesium transporter gene OsMGT1 is required for conferring aluminum tolerance in rice. Plant Physiol. 159: 1624-1633.
3. Chen, J., Li, L.G., Liu, Z.H., Yuan, Y.J., Guo, L.L., Tian, L.F. et al. (2009) Magnesium transporter AtMGT9 is essential for pollen development in Arabidopsis. Cell Res. 19: 887-898.
4. Chen, S., Tao, L., Zeng, L., Vega-Sanchez, M.E., Umemura, K. and Wang, G.L. (2006) A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice. Mol. Plant Pathol. 7: 417-427. (Pubitemid 44337800)
5. Conn, S.J., Conn, V., Tyerman, S.D., Kaiser, B.N., Leigh, R.A. and 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.
6. Deng, W., Luo, K., Li, D., Zheng, X., Wei, X., Smith, W. et al. (2006) Overexpression of an Arabidopsis magnesium transport gene, AtMGT1, in Nicotiana benthamiana confers Al tolerance. J. Exp. Bot. 57: 4235-4243. (Pubitemid 44950420)
7. Drummond, R.S.M., Tutone, A., Li, Y.C. and Gardner, R.C. (2006) A putative magnesium transporter AtMRS2-11 is localized to the plant chloroplast envelope membrane system. Plant Sci. 170: 78-89. (Pubitemid 41501422)
8. Eshaghi, S., Niegowski, D., Kohl, A., Molina, D.M., Lesley, S.A. and Nordlund, P. (2006) Crystal structure of a divalent metal ion transporter CorA at 2.9 angstrom resolution. Science 313: 354-357. (Pubitemid 44480960)
9. Froehlich, J.E., Wilkerson, C.G., Ray, W.K., McAndrew, R.S., Osteryoung, K.W., Gage, D.A. et al. (2003) Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. J. Proteome Res. 2: 413-425. (Pubitemid 36988420)
10. Gebert, M., Meschenmoser, K., Svidova, S., Weghuber, J., Schweyen, R., Eifler, K. et al. (2009) A root-expressed magnesium transporter of the MRS2/MGTgene family in Arabidopsis thaliana allows for growth in low-Mg2+ environments. Plant Cell 21: 4018-4030.
11. Guskov, A., Nordin, N., Reynaud, A., Engman, H., Lundbäck, A., Jong, A.J.O. et al. (2012) Structural insights into the mechanisms of Mg2+ uptake, transport, and gating by CorA. Proc. Natl Acad. Sci. USA 109: 18459-18464.
12. Ishijima, S., Uchlbori, A., Takagi, H., Maki, R. and Ohnishi, M. (2003) Light-induced increase in free Mg2+ concentration in spinach chloroplasts: measurement of free Mg2+ by using a fluorescent probe and necessity of stromal alkalinization. Arch. Biochem. Biophys. 412: 126-132. (Pubitemid 36324372)
13. Iwata, R., Kawamura, M., Ido, T. and Kimura, S. (1992) Chromatographic purification of no-carrier-added magnesium-28 for biological studies. J. Radioanal. Nucl. Chem. 159: 233-237.
14. Kikuchi, S., Satoh, K., Nagata, T., Kawagashira, N., Doi, K., Kishimoto, N. et al. (2003) Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301: 376-379. (Pubitemid 36877074)
15. Knoop, V., Groth-Malonek, M., Gebert, M., Eifler, K. and Weyand, K. (2005) Transport of magnesium and other divalent cations: evolution of the 2-TM-GxN proteins in the MIT superfamily. Mol. Genet. Genomics 274: 205-216. (Pubitemid 41476767)
16. Kolisek, M., Zsurka, G., Samaj, J., Weghuber, J., Schweyen, R.J. and Schweigel, M. (2003) Mrs2p is an essential component of the major electrophoretic Mg2+ influx system in mitochondria. EMBO J. 22: 1235-1244. (Pubitemid 36362687)
17. Li, L., Sokolov, L.N., Yang, Y., Li, D., Ting, J., Pandy, G.K. et al. (2008) A mitochondrial magnesium transporter functions in Arabidopsis pollen development. Mol. Plant. 1: 675-685.
18. Li, L., Tutone, A.F., Drummond, R.S., Gardner, R.C. and Luan, S. (2001) A novel family of magnesium transport genes in Arabidopsis. Plant Cell 13: 2761-2775. (Pubitemid 34088639)
19. Lunin, V.V., Dobrovetsky, E., Khutoreskaya, G., Zhang, R., Joachimiak, A., Doyle, D.A. et al. (2006) Crystal structure of the CorA Mg2+ transporter. Nature 440: 833-837.
20. Maguire, M.E. and Cowan, J.A. (2002) Magnesium chemistry and biochemistry. BioMetals 15: 203-210. (Pubitemid 34816205)
21. Mao, D.D., Tian, L.F., Li, L.G., Chen, J., Deng, P.Y., Li, D.P. et al. (2008) AtMGT7: an Arabidopsis gene encoding a low-affinity magnesium transporter. J. Integr. Plant Biol. 50: 1530-1538.
22. Mikosch, M., Käberich, K. and Homann, U. (2009) ER export of KAT1 is correlated to the number of acidic residues within a triacidic motif. Traffic 10: 1481-1487.
23. Moomaw, A.S. and Maguire, M.E. (2008) The unique nature of Mg2+ channels. Physiology 23: 275-285.
24. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y. et al. (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104: 34-41. (Pubitemid 47223816)
25. Nicholas, K.B., Nicholas, H.B. and Deerfield, D.W. (1997) GeneDoc: analysis and visualization of genetic variation. EMBNEW. NEWS 4: 14.
26. Niegowski, D. and Eshaghi, S. (2007) The CorA family: structure and function revisited. Cell. Mol. Life Sci 64: 2564-2574. (Pubitemid 350035607)
27. Ohyanagi, H., Tanaka, T., Sakai, H., Shigemoto, Y., Yamaguchi, K., Habara, T. et al. (2006) The Rice Annotation Project Database (RAP-DB): hub for Oryza sativa ssp. japonica genome information. Nucleic Acids Res. 34: 741-744.
28. Payandeh, J., Li, C., Ramjeesingh, M., Poduch, W., Bear, C.E. and Pai, E.F. (2008) Probing structure-function relationships and gating mechanisms in the CorA Mg2+ transport system. J. Biol. Chem. 283: 11721-11733.
29. Payandeh, J. and Pai, E.F. (2006) A structural basis for Mg2+ homeostasis and the CorA translocation cycle. EMBO J. 25: 3762-3773. (Pubitemid 44300262)
30. Portis, A.R. (1981) Evidence of a low stromal Mg2+ concentration in intact chloroplasts in the dark. Plant Physiol. 67: 985-989.
31. Sato, Y., Antonio, B.A., Namiki, N., Motoyama, R., Sugimoto, K., Takehisa, H. et al. (2011) Field transcriptome revealed critical developmental and physiological transitions involved in the expression of growth potential in japonica rice. BMC Plant Biol. 11: 10.
32. Schock, I., Gregan, J., Steinhauser, S., Schweyen, R., Brennicke, A. and 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. (Pubitemid 32003674)
33. Shaul, O. (2002) Magnesium transport and function in plants: the tip of the iceberg. BioMetals 15: 309-323. (Pubitemid 34816214)
34. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
35. Tanoi, K., Saito, T., Iwata, N., Kobayashi, N.I. and Nakanishi, T.M. (2011) The analysis of magnesium transport system from external solution to xylem in rice root. Soil Sci. Plant Nutr. 57: 265-271.
36. Worlock, A.J. and Smith, R.L. (2002) ZntB is a novel Zn2+ transporter in Salmonella enterica serovar typhimurium. J. Bacteriol. 184: 4369-4373. (Pubitemid 34832564)
37. Xia, Y., Lundbäck, A., Sahaf, N., Nordlund, G., Brzezinski, P. and Eshaghi, S. (2011) Co2+ selectivity of Thermotoga maritima CorA and its inability to regulate Mg2+ homeostasis present a new class of CorA proteins. J. Biol. Chem. 286: 16525-16532.
38. Zybailov, B., Rutschow, H., Friso, G., Rudella, A., Emanuelsson, O., Sun, Q. et al. (2011) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One 3: e1994.