title: Medicago truncatula natural resistance-associated macrophage Protein1 is required for iron uptake by rhizobia-infected nodule cells.
abstract: Iron is critical for symbiotic nitrogen fixation (SNF) as a key component of multiple ferroproteins involved in this biological process. In the model legume Medicago truncatula, iron is delivered by the vasculature to the infection/maturation zone (zone II) of the nodule, where it is released to the apoplast. From there, plasma membrane iron transporters move it into rhizobia-containing cells, where iron is used as the cofactor of multiple plant and rhizobial proteins (e.g. plant leghemoglobin and bacterial nitrogenase). MtNramp1 (Medtr3g088460) is the M. truncatula Natural Resistance-Associated Macrophage Protein family member, with the highest expression levels in roots and nodules. Immunolocalization studies indicate that MtNramp1 is mainly targeted to the plasma membrane. A loss-of-function nramp1 mutant exhibited reduced growth compared with the wild type under symbiotic conditions, but not when fertilized with mineral nitrogen. Nitrogenase activity was low in the mutant, whereas exogenous iron and expression of wild-type MtNramp1 in mutant nodules increased nitrogen fixation to normal levels. These data are consistent with a model in which MtNramp1 is the main transporter responsible for apoplastic iron uptake by rhizobia-infected cells in zone II.
authors.affiliation: Centro de Biotecnología y Genómica de Plantas, Campus de Montegancedo, Universidad Politécnica de Madrid, 28223 Madrid, Spain (M.T.-J., R.C.-R., J.I., M.G.-G.);Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (I.K., M.U.);Instituto de Ciencias Agrarias, Consejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (M.M.L.); andConsejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (J.I.).
authors.forename: Manuel
authors.initials: M
authors.lastname: Tejada-Jiménez
authors.affiliation: Centro de Biotecnología y Genómica de Plantas, Campus de Montegancedo, Universidad Politécnica de Madrid, 28223 Madrid, Spain (M.T.-J., R.C.-R., J.I., M.G.-G.);Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (I.K., M.U.);Instituto de Ciencias Agrarias, Consejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (M.M.L.); andConsejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (J.I.).
authors.forename: Rosario
authors.initials: R
authors.lastname: Castro-Rodríguez
authors.affiliation: Centro de Biotecnología y Genómica de Plantas, Campus de Montegancedo, Universidad Politécnica de Madrid, 28223 Madrid, Spain (M.T.-J., R.C.-R., J.I., M.G.-G.);Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (I.K., M.U.);Instituto de Ciencias Agrarias, Consejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (M.M.L.); andConsejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (J.I.).
authors.forename: Igor
authors.initials: I
authors.lastname: Kryvoruchko
authors.affiliation: Centro de Biotecnología y Genómica de Plantas, Campus de Montegancedo, Universidad Politécnica de Madrid, 28223 Madrid, Spain (M.T.-J., R.C.-R., J.I., M.G.-G.);Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (I.K., M.U.);Instituto de Ciencias Agrarias, Consejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (M.M.L.); andConsejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (J.I.).
authors.forename: M Mercedes
authors.initials: MM
authors.lastname: Lucas
authors.affiliation: Centro de Biotecnología y Genómica de Plantas, Campus de Montegancedo, Universidad Politécnica de Madrid, 28223 Madrid, Spain (M.T.-J., R.C.-R., J.I., M.G.-G.);Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (I.K., M.U.);Instituto de Ciencias Agrarias, Consejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (M.M.L.); andConsejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (J.I.).
authors.forename: Michael
authors.initials: M
authors.lastname: Udvardi
authors.affiliation: Centro de Biotecnología y Genómica de Plantas, Campus de Montegancedo, Universidad Politécnica de Madrid, 28223 Madrid, Spain (M.T.-J., R.C.-R., J.I., M.G.-G.);Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (I.K., M.U.);Instituto de Ciencias Agrarias, Consejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (M.M.L.); andConsejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (J.I.).
authors.forename: Juan
authors.initials: J
authors.lastname: Imperial
authors.affiliation: Centro de Biotecnología y Genómica de Plantas, Campus de Montegancedo, Universidad Politécnica de Madrid, 28223 Madrid, Spain (M.T.-J., R.C.-R., J.I., M.G.-G.);Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (I.K., M.U.);Instituto de Ciencias Agrarias, Consejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (M.M.L.); andConsejo Superior de Investigaciones Científicas, 28006 Madrid, Spain (J.I.) manuel.gonzalez@upm.es.
authors.forename: Manuel
authors.initials: M
authors.lastname: González-Guerrero
mesh_terms: D001692:Biological Transport / Q000187:drug effects; D027682:Cation Transport Proteins / Q000235:genetics / Q000378:metabolism*; D002462:Cell Membrane / Q000187:drug effects / Q000378:metabolism; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D055786:Gene Knockout Techniques; D005816:Genetic Complementation Test; D007501:Iron / Q000378:metabolism* / Q000494:pharmacology; D008345:Manganese / Q000378:metabolism; D046913:Medicago truncatula / Q000235:genetics / Q000378:metabolism* / Q000382:microbiology*; D008954:Models, Biological; D005810:Multigene Family; D016254:Mutagenesis, Insertional / Q000235:genetics; D009591:Nitrogenase / Q000378:metabolism; D010641:Phenotype; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D011401:Promoter Regions, Genetic / Q000235:genetics; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D012231:Rhizobium / Q000187:drug effects / Q000502:physiology*; D053204:Root Nodules, Plant / Q000187:drug effects / Q000378:metabolism / Q000382:microbiology*; D013347:Subcellular Fractions / Q000187:drug effects / Q000378:metabolism; D013559:Symbiosis / Q000187:drug effects; D014158:Transcription, Genetic / Q000187:drug effects; D000099173:Natural Resistance-associated Macrophage Protein 1
chemical_list: D027682:Cation Transport Proteins; D007501:Iron; D008345:Manganese; D009591:Nitrogenase; D010940:Plant Proteins; D012333:RNA, Messenger; D000099173:Natural Resistance-associated Macrophage Protein 1
references.citation: Front Plant Sci. 2014 Feb 13;5:45
references.pmid: 24592271
references.citation: Mol Plant Microbe Interact. 2000 Nov;13(11):1204-13
references.pmid: 11059487
references.citation: Nat Rev Microbiol. 2013 Apr;11(4):252-63
references.pmid: 23493145
references.citation: J Bacteriol. 1996 Mar;178(6):1532-8
references.pmid: 8626278
references.citation: New Phytol. 2009;181(3):637-50
references.pmid: 19054339
references.citation: Curr Biol. 2005 Mar 29;15(6):531-5
references.pmid: 15797021
references.citation: Nucleic Acids Res. 1985 Jul 11;13(13):4777-88
references.pmid: 4022773
references.citation: Biochem J. 2009 Aug 13;422(2):217-28
references.pmid: 19545236
references.citation: Mol Plant Microbe Interact. 2001 Jun;14(6):695-700
references.pmid: 11386364
references.citation: Plant J. 2009 Apr;58(2):195-207
references.pmid: 19121106
references.citation: New Phytol. 1992 Jul;121(3):457-467
references.pmid: 33874148
references.citation: Plant J. 2007 Sep;51(6):1126-36
references.pmid: 17666025
references.citation: Mol Cell Biol. 2000 Nov;20(21):7893-902
references.pmid: 11027260
references.citation: Proc Natl Acad Sci U S A. 2000 Apr 25;97(9):4991-6
references.pmid: 10781110
references.citation: J Biol Chem. 1994 Oct 21;269(42):26092-9
references.pmid: 7929320
references.citation: J Bacteriol. 1994 Sep;176(17):5297-303
references.pmid: 8071205
references.citation: Plant Physiol. 2003 Mar;131(3):872-7
references.pmid: 12644639
references.citation: Biochim Biophys Acta. 1993 Apr 21;1163(1):31-41
references.pmid: 8386550
references.citation: Mol Plant Microbe Interact. 2007 Mar;20(3):262-75
references.pmid: 17378429
references.citation: Curr Opin Plant Biol. 2008 Apr;11(2):166-70
references.pmid: 18314378
references.citation: Plant Cell Physiol. 2013 Apr;54(4):585-94
references.pmid: 23385147
references.citation: Methods Mol Biol. 2011;678:179-90
references.pmid: 20931380
references.citation: Cell. 1994 Jan 28;76(2):403-10
references.pmid: 8293473
references.citation: Plant Mol Biol. 1997 Apr;33(6):1085-92
references.pmid: 9154989
references.citation: Plant Physiol. 2010 Apr;152(4):1986-99
references.pmid: 20181755
references.citation: Electrophoresis. 2009 Jun;30 Suppl 1:S162-73
references.pmid: 19517507
references.citation: J Bacteriol. 1998 Oct;180(19):5183-91
references.pmid: 9748453
references.citation: Plant J. 2003 Mar;33(5):949-56
references.pmid: 12609035
references.citation: Front Plant Sci. 2013 Sep 13;4:359
references.pmid: 24062758
references.citation: Metallomics. 2013 Sep;5(9):1247-53
references.pmid: 23765084
references.citation: Curr Genet. 1989 Dec;16(5-6):339-46
references.pmid: 2692852
references.citation: Plant Cell. 2002 Jun;14(6):1223-33
references.pmid: 12084823
references.citation: Biochim Biophys Acta. 2006 Jul;1763(7):609-20
references.pmid: 16908340
references.citation: Biochim Biophys Acta. 2006 Jul;1763(7):595-608
references.pmid: 16857279
references.citation: Biometals. 2005 Feb;18(1):107-20
references.pmid: 15865416
references.citation: Plant J. 2014 Mar;77(6):817-37
references.pmid: 24483147
references.citation: EMBO J. 2005 Dec 7;24(23):4041-51
references.pmid: 16270029
references.citation: Plant Physiol Biochem. 2009 Nov-Dec;47(11-12):1082-8
references.pmid: 19716309
references.citation: Nucleic Acids Res. 2014 Jan;42(Database issue):D251-8
references.pmid: 24225317
references.citation: Microbiol Rev. 1995 Mar;59(1):124-42
references.pmid: 7708010
references.citation: Plant Cell. 2010 Mar;22(3):904-17
references.pmid: 20228245
references.citation: Trends Microbiol. 2001 Aug;9(8):397-403
references.pmid: 11514223
references.citation: EMBO J. 1987 Dec 20;6(13):3901-7
references.pmid: 3327686
references.citation: Biochim Biophys Acta. 1966 Oct 31;127(2):285-94
references.pmid: 5964974
references.citation: Curr Biol. 2014 Mar 3;24(5):R184-90
references.pmid: 24602880
references.citation: J Biosci Bioeng. 2007 Jul;104(1):34-41
references.pmid: 17697981
references.citation: Mol Microbiol. 2010 Dec;78(5):1246-58
references.pmid: 21091508
references.citation: J Bacteriol. 1990 Aug;172(8):4295-306
references.pmid: 2376562
references.citation: Plant J. 2003 Aug;35(3):295-304
references.pmid: 12887581
references.citation: Plant Cell Physiol. 2012 Jan;53(1):225-36
references.pmid: 22123791
references.citation: Plant Physiol. 1996 Jul;111(3):893-900
references.pmid: 12226335
references.citation: Eur J Cell Biol. 1989 Jun;49(1):13-23
references.pmid: 2759097
references.citation: Annu Rev Plant Biol. 2013;64:781-805
references.pmid: 23451778
references.citation: PLoS One. 2013 Dec 31;8(12):e83990
references.pmid: 24391861
references.citation: Nat Struct Mol Biol. 2014 Nov;21(11):990-6
references.pmid: 25326704
references.citation: Plant Physiol. 1968 Aug;43(8):1185-207
references.pmid: 16656902
references.citation: Plant J. 2008 Apr;54(2):335-47
references.pmid: 18208518
references.citation: Plant Physiol Biochem. 2005 Aug;43(8):793-801
references.pmid: 16198592
references.citation: Biochem Biophys Res Commun. 1979 Jan 30;86(2):259-64
references.pmid: 426786
references.citation: New Phytol. 2007;174(1):11-25
references.pmid: 17335493
references.citation: Biochem J. 2000 May 1;347 Pt 3:749-55
references.pmid: 10769179
references.citation: Proc Natl Acad Sci U S A. 1996 May 14;93(10):5105-10
references.pmid: 8643535
references.citation: Annu Rev Cell Biol. 1991;7:191-226
references.pmid: 1809347
references.citation: Nat Commun. 2013;4:2442
references.pmid: 24048172