Medicago truncatula Ferroportin2 mediates iron import into nodule symbiosomes.
ferroportin
iron
iron transport
nitrogenase
nodulation
symbiotic nitrogen fixation
transition metal nutrition
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
10 2020
10 2020
Historique:
received:
25
11
2019
accepted:
27
04
2020
pubmed:
6
5
2020
medline:
15
5
2021
entrez:
6
5
2020
Statut:
ppublish
Résumé
Iron is an essential cofactor for symbiotic nitrogen fixation, required by many of the enzymes involved, including signal transduction proteins, O
Substances chimiques
Plant Proteins
0
Iron
E1UOL152H7
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
194-209Informations de copyright
© 2020 The Authors New Phytologist © 2020 New Phytologist Trust.
Références
Almagro-Armenteros JJ, Sønderby CK, Sønderby SK, Nielsen H, Winther O. 2017. DeepLoc: prediction of protein subcellular localization using deep learning. Bioinformatics 33: 3387-3395.
Andaluz S, Rodríguez-Celma J, Abadía A, Abadía J, López-Millán AF. 2009. Time course induction of several key enzymes in Medicago truncatula roots in response to Fe deficiency. Plant Physiology and Biochemistry 47: 1082-1088.
Appleby CA. 1984. Leghemoglobin and Rhizobium respiration. Annual Review of Plant Physiology 35: 443-478.
Arpat AB, Magliano P, Wege S, Rouached H, Stefanovic A, Poirier Y. 2012. Functional expression of PHO1 to the Golgi and trans-Golgi network and its role in export of inorganic phosphate. The Plant Journal 71: 479-491.
Boisson-Dernier A, Chabaud M, Garcia F, Bécard G, Rosenberg C, Barker DG. 2001. Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Molecular Plant-Microbe Interactions 14: 695-700.
Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
Braunschweig J, Bosch J, Heister K, Kuebeck C, Meckenstock RU. 2012. Reevaluation of colorimetric iron determination methods commonly used in geomicrobiology. Journal of Microbiological Methods 89: 41-48.
Brear EM, Bedon F, Gavrin A, Kryvoruchko IS, Torres-Jerez I, Udvardi MK, Day DA, Smith PMC. 2020. GmVTL1 is an iron transporter on the symbiosome membrane of soybean with an important role in nitrogen fixation. BioRxiv. doi: 10.1101/2020.03.03.975805.
Brear EM, Day DA, Smith PMC. 2013. Iron: an essential micronutrient for the legume-rhizobium symbiosis. Frontiers in Plant Science 4: 359.
Brito B, Palacios JM, Hidalgo E, Imperial J, Ruíz-Argüeso T. 1994. Nickel availability to pea (Pisum sativum L.) plants limits hydrogenase activity of Rhizobium leguminosarum bv. viciae bacteroids by affecting the processing of the hydrogenase structural subunits. Journal of Bacteriology 176: 5297-5303.
Cheng HP, Walker GC. 1998. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. Journal of Bacterology 180: 5183-5191.
Colangelo EP, Guerinot ML. 2004. The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16: 3400-3412.
Conte S, Stevenson D, Furner I, Lloyd A. 2009. Multiple antibiotic resistance in Arabidopsis is conferred by mutations in a chloroplast-localized transport protein. Plant Physiology 151: 559.
Cotte MPE, Salomé M, Rivard C, Nolf WD, Castillo-Michel H, Fabris T, Monico L, Janssens K, Wang T, Sciau P et al. 2017. The ID21 X-ray and infrared microscopy beamline at the ESRF: status and recent applications to artistic materials. Journal of Analytical Atomic Spectrometry 32: 477-493.
Couzigou JM, Zhukov V, Mondy S, Abu el Heba G, Cosson V, Ellis TH, Ambrose M, Wen J, Tadege M, Tikhonovich I et al. 2012. NODULE ROOT and CHOCHLEATA maintain nodule development and are legume orthologs of Arabidopsis BLADE-ON-PETIOLE genes. Plant Cell 24: 4498-4510.
Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL. 2001. Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409: 346-349.
Dalton DA, Joyner SL, Becana M, Iturbe-Ormaetxe I, Chatfield JM. 1998. Antioxidant defenses in the peripheral cell layers of legume root nodules. Plant Physiology 116: 37-43.
Demsar J, Curk T, Erjavec A, Gorup C, Hocevar T, Milutinovic M, Mozina M, Polajnar M, Toplak M, Staric A et al. 2013. Orange: data mining toolbox in Python. Journal of Machine Learning Research 14: 2349-2353.
Deshpande CN, Ruwe TA, Shawki A, Xin V, Vieth KR, Valore EV, Qiao B, Ganz T, Nemeth E, Mackenzie B et al. 2018. Calcium is an essential cofactor for metal efflux by the ferroportin transporter family. Nature Communications 9: 3075.
Downie JA. 2014. Legume nodulation. Current Biology 24: R184-R190.
Drakesmith H, Nemeth E, Ganz T. 2015. Ironing out Ferroportin. Cell Metabolism 22: 777-787.
Durrett TP, Gassmann W, Rogers EE. 2007. The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiology 144: 197-205.
Flis P, Ouerdane L, Grillet L, Curie C, Mari S, Lobinski R. 2016. Inventory of metal complexes circulating in plant fluids: a reliable method based on HPLC coupled with dual elemental and high-resolution molecular mass spectrometric detection. New Phytologist 211: 1129-1141.
Gage DJ. 2002. Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti. Journal of Bacteriology 184: 7042-7046.
Goldstein S, Meyerstein D, Czapski G. 1993. The Fenton reagents. Free Radical Biology and Medicine 15: 435-445.
González-Guerrero M, Escudero V, Sáez Á, Tejada-Jiménez M. 2016. Transition metal transport in plants and associated endosymbionts. Arbuscular mycorrhizal fungi and rhizobia. Frontiers in Plant Science 7: 1088.
González-Guerrero M, Matthiadis A, Sáez Á, Long TA. 2014. Fixating on metals: new insights into the role of metals in nodulation and symbiotic nitrogen fixation. Frontiers in Plant Science 5: 45.
González-Guerrero M, Raimunda D, Cheng X, Argüello JM. 2010. Distinct functional roles of homologous Cu+ efflux ATPases in Pseudomonas aeuginosa. Molecular Microbiology 78: 1246-1258.
Grillet L, Lan P, Li W, Mokkapati G, Schmidt W. 2018. IRON MAN is a ubiquitous family of peptides that control iron transport in plants. Nature Plants 4: 953-963.
Hakoyama T, Niimi K, Yamamoto T, Isobe S, Sato S, Nakamura Y, Tabata S, Kumagai H, Umehara Y, Brossuleit K et al. 2012. The integral membrane protein SEN1 is required for symbiotic nitrogen fixation in Lotus japonicus nodules. Plant and Cell Physiology 53: 225-236.
Hardy RW, Holsten RD, Jackson EK, Burns RC. 1968. The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiology 43: 1185-1207.
Herridge DF, Peoples MB, Boddey RM. 2008. Global inputs of biological nitrogen fixation in agricultural systems. Plant and Soil 311: 1-18.
Hirschi KD. 2009. Nutrient biofortification of food crops. Annual Review of Nutrition 29: 401-421.
Huisman R, Ovchinnikova E, Bisseling T, Limpens E. 2012. Endocytic accommodation of microbes in plants. In: Samaj J, ed. Endocytosis in plants. Berlin/Heidelberg: Springer-Verlag, 271-295.
Kaiser BN, Moreau S, Castelli J, Thomson R, Lambert A, Bogliolo S, Puppo A, Day DA. 2003. The soybean NRAMP homologue, GmDMT1, is a symbiotic divalent metal transporter capable of ferrous iron transport. The Plant Journal 35: 295-304.
Kaplan J. 2002. Mechanisms of cellular iron acquisition: another iron in the fire. Cell 111: 603-606.
Kereszt A, Mergaert P, Kondorosi E. 2011. Bacteroid development in legume nodules: evolution of mutual benefit or of sacrificial victims? Molecular Plant-Microbe Interactions 24: 1300-1309.
Kobayashi T, Nishizawa NK. 2012. Iron uptake, translocation, and regulation in higher plants. Annual Review of Plant Biology 63: 131-152.
Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB. 1999. The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Molecular Biology 40: 37-44.
Kryvoruchko IS, Routray P, Sinharoy S, Torres-Jerez I, Tejada-Jiménez M, Finney LA, Nakashima J, Pislariu CI, Benedito VA, González-Guerrero M et al. 2018. An iron-activated citrate transporter, MtMATE67, is required for symbiotic nitrogen fixation. Plant Physiology 176: 2315-2329.
Kumar RK, Chu HH, Abundis C, Vasques K, Rodriguez DC, Chia JC, Huang R, Vatamaniuk OK, Walker EL. 2017. Iron-nicotianamine transporters are required for proper long distance iron signaling. Plant Physiology 175: 1254.
Le Vier K, Day DA, Guerinot ML. 1996. Iron uptake by symbiosomes from soybean root nodules. Plant Physiology 111: 893-900.
Li L, Chen OS, Ward DM, Kaplan J. 2001. CCC1 is a transporter that mediates vacuolar iron storage in yeast. Journal of Biological Chemistry 276: 29515-29519.
Limpens E, Ivanov S, van Esse W, Voets G, Fedorova E, Bisseling T. 2009. Medicago N2-fixing symbiosomes acquire the endocytic identity marker Rab7 but delay the acquisition of vacuolar identity. Plant Cell 21: 2811-2828.
Lin H, Li L, Jia X, Ward DM, Kaplan J. 2011. Genetic and biochemical analysis of high iron toxicity in yeast: iron toxicity is due to the accumulation of cytosolic iron and occurs under both aerobic and anaerobic conditions. Journal of Biological Chemistry 286: 3851-3862.
Liu S, Liao LL, Nie MM, Peng WT, Zhang MS, Lei JN, Zhong YJ, Liao H, Chen ZC. 2020. A VIT-like transporter facilitates iron transport into nodule symbiosomes for nitrogen fixation in soybean. New Phytologist 226: 1413-1428
Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN. 2010. The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 22: 2219-2236.
López-Millán AF, Morales FN, Abadı́a A, Abadı́a J. 2000. Effects of iron deficiency on the composition of the leaf apoplastic fluid and xylem sap in sugar beet. Implications for iron and carbon transport. Plant Physiology 124: 873-884.
Manceau A, Marcus M, Lenoir T. 2014. Estimating the number of pure chemical components in a mixture by X-ray absorption spectroscopy. Journal of Synchrotron Radiation 21: 1140-1147.
Marschner P. 2011. Mineral nutrition of higher plants, 3rd edn. Amsterdam, the Netherlands: Academic Press.
McKie AT, Marciani P, Rolfs A, Brennan K, Wehr K, Barrow D, Miret S, Bomford A, Peters TJ, Farzaneh F et al. 2000. A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Molecular Cell 5: 299-309.
Montiel J, Arthikala MK, Cárdenas L, Quinto C. 2016. Legume NADPH oxidases have crucial roles at different stages of nodulation. International Journal of Molecular Sciences 17: 680.
Montiel J, Nava N, Cárdenas L, Sánchez-López R, Arthikala MK, Santana O, Sánchez F, Quinto C. 2012. A Phaseolus vulgaris NADPH oxidase gene is required for root infection by rhizobia. Plant and Cell Physiology 53: 1751-1767.
Moreau S, Meyer JM, Puppo A. 1995. Uptake of iron by symbiosomes and bacteroids from soybean nodules. FEBS Letters 361: 225-228.
Morrissey J, Baxter IR, Lee J, Li L, Lahner B, Grotz N, Kaplan J, Salt DE, Guerinot ML. 2009. The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21: 3326-3338.
Mus F, Crook MB, Garcia K, Garcia Costas A, Geddes BA, Kouri ED, Paramasivan P, Ryu MH, Oldroyd GE, Poole PS et al. 2016. Symbiotic nitrogen fixation and challenges to extending it to non-legumes. Applied and Environmental Microbiology 82: 3698-3710.
Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T. 2007. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. Journal of Bioscience and Bioengineering 104: 34-41.
Nelson MS, Sadowsky MJ. 2015. Secretion systems and signal exchange between nitrogen-fixing rhizobia and legumes. Frontiers in Plant Science 6: 491.
Nevo Y, Nelson N. 2006. The NRAMP family of metal-ion transporters. Biochimica et Biophysica Acta 1763: 609-620.
O'Hara GW, Dilworth MJ, Boonkerd N, Parkpian P. 1988. Iron-deficiency specifically limits nodule development in peanut inoculated with Bradyrhizobium sp. New Phytologist 108: 51-57.
Oldroyd GE. 2013. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Reviews Microbiology 11: 252-263.
Oldroyd GE, Dixon R. 2014. Biotechnological solutions to the nitrogen problem. Current Opinion in Biotechnology. 26: 19-24.
Preisig O, Zufferey R, Hennecke H. 1996a. The Bradyrhizobium japonicum fixGHIS genes are required for the formation of the high-affinity cbb(3)-type cytochrome oxidase. Archives of Microbiology 165: 297-305.
Preisig O, Zufferey R, Thony-Meyer L, Appleby C, Hennecke H. 1996b. A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. Journal of Bacteriology 178: 1532-1538.
Raul B, Kryvoruchko I, Benedito VA, Bandyopadhyay K, Sinharoy S. 2019. Root nodule development in model versus non-canonical plants. In: Khurana S, Gaur R, eds. Plant biotechnology: progress in genomic Era. Singapore: Springer, 397-428.
Rodríguez-Celma J, Lin WD, Fu GM, Abadía J, López-Millán AF, Schmidt W. 2013. Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula. Plant Physiology 162: 1473-1485.
Rodríguez-Haas B, Finney L, Vogt S, González-Melendi P, Imperial J, González-Guerrero M. 2013. Iron distribution through the developmental stages of Medicago truncatula nodules. Metallomics 5: 1247-1253.
Rogers EE, Guerinot ML. 2002. FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14: 1787-1799.
Roschzttardtz H, Séguéla-Arnaud M, Briat JF, Vert G, Curie C. 2011. The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout Arabidopsis development. Plant Cell 23: 2725-2737.
Roux B, Rodde N, Jardinaud MF, Timmers T, Sauviac L, Cottret L, Carrère S, Sallet E, Courcelle E, Moreau S et al. 2014. An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing. The Plant Journal 77: 817-837.
Rubio LM, Ludden PW. 2005. Maturation of nitrogenase: a biochemical puzzle. Journal of Bacteriology 187: 405-414.
Rubio MC, James EK, Clemente MR, Bucciarelli B, Fedorova M, Vance CP, Becana M. 2004. Localization of superoxide dismutases and hydrogen peroxide in legume root nodules. Molecular Plant-Microbe Interactions 17: 1294-1305.
Schiestl RH, Gietz RD. 1989. High efficiency transformation of intact yeast cells using single stranded nucleic acids as carrier. Current Genetics 16: 339-346.
Sivitz AB, Hermand V, Curie C, Vert G. 2012. Arabidopsis bHLH100 and bHLH101 control iron homeostasis via a FIT-independent pathway. PLoS ONE 7: e44843.
Solé VA, Papillon E, Cotte M, Walter P, Susini JA. 2007. A multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra. Spectrochimica Acta Part B: Atomic Spectroscopy 62: 63-68.
Sprent JI. 2007. Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytologist 174: 11-25.
Stephens B, Cook D, Grusak M. 2011. Characterization of zinc transport by divalent metal transporters of the ZIP family from the model legume Medicago truncatula. BioMetals 24: 51-58.
Sutton WD, Pankhurst CE, Craig AS. 1981. The Rhizobium bacteroid state. In: Atherly KL, Gilesalan G, eds. Biology of the Rhizobiaceae. New York, NY, USA: Academic Press, 149-177.
Tadege M, Wen J, He J, Tu H, Kwak Y, Eschstruth A, Cayrel A, Endre G, Zhao PX, Chabaud M et al. 2008. Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. The Plant Journal. 54: 335-347.
Tang C, Robson AD, Dilworth MJ. 1990. The role of iron in nodulation and nitrogen fixation in Lupinus angustifolius L. New Phytologist 114: 173-182.
Tang C, Robson AD, Dilworth MJ, Kuo J. 1992. Microscopic evidence on how iron-deficiency limits nodule initiation in Lupinus angustifolius L. New Phytologist 121: 457-467.
Taniguchi R, Kato HE, Font J, Deshpande CN, Wada M, Ito K, Ishitani R, Jormakka M, Nureki O. 2015. Outward- and inward-facing structures of a putative bacterial transition-metal transporter with homology to ferroportin. Nature Communications 6: 8545.
Tejada-Jiménez M, Castro-Rodríguez R, Kryvoruchko I, Lucas MM, Udvardi M, Imperial J, González-Guerrero M. 2015. Medicago truncatula natural resistance-associated macrophage Protein1 is required for iron uptake by rhizobia-infected nodule cells. Plant Physiology 168: 258-272.
Tejada-Jiménez M, Gil-Diez P, León-Mediavilla J, Wen J, Mysore KS, Imperial J, González-Guerrero M. 2017. Medicago truncatula molybdate transporter type 1 (MOT1.3) is a plasma membrane molybdenum transporter required for nitrogenase activity in root nodules under molybdenum deficiency. New Phytologist 216: 1223-1235.
Terry RE, Soerensen KU, Jolley VD, Brown JC. 1991. The role of active Bradyrhizobium japonicum in iron stress response of soy-beans. Plant and Soil 130: 225-230.
Timmers ACJ, Soupène E, Auriac MC, de Billy F, Vasse J, Boistard P, Truchet G. 2000. Saprophytic intracellular rhizobia in alfalfa nodules. Molecular Plant-Microbe Interactions 13: 1204-1213.
Udvardi MK, Poole PS. 2013. Transport and metabolism in legume-rhizobia symbioses. Annual Review of Plant Biology 64: 781-805.
Vance CP. 2001. Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiology 127: 390-397.
Vasse J, de Billy F, Camut S, Truchet G. 1990. Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. Journal of Bacteriology 172: 4295-4306.
Vernoud V, Journet EP, Barker DG. 1999. MtENOD20, a Nod factor-inducible molecular marker for root cortical cell activation. Molecular Plant-Microbe Interactions 12: 604-614.
Vert G, Grotz N, Dedaldéchamp F, Gaymard F, Guerinot ML, Briat JF, Curie C. 2002. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and the plant growth. Plant Cell 14: 1223-1233.
Walton JH, Kontra-Kováts G, Green RT, Domonkos A, Horváth B, Brear EM, Franceschetti M, Kaló P, Balk J. 2019. The Medicago truncatula vacuolar iron transporter-like proteins VTL4 and VTL8 deliver iron to endosymbiotic bacteria at different stages of the infection process. BioRxiv. doi: 10.1101/689224
White PJ, Broadley MR. 2009. Biofortification of crops with seven mineral elements often lacking in human diets - iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytologist 182: 49-84.
von Wiren N, Klair S, Bansal S, Briat JF, Khodr H, Shioiri T, Leigh RA, Hider RC. 1999. Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants. Plant Physiology 119: 1107-1114.
Xiao TT, Schilderink S, Moling S, Deinum EE, Kondorosi E, Franssen H, Kulikova O, Niebel A, Bisseling T. 2014. Fate map of Medicago truncatula root nodules. Development 141: 3517-3528.
Zhai Z, Gayomba SR, Jung HI, Vimalakumari NK, Piñeros M, Craft E, Rutzke MA, Danku J, Lahner B, Punshon T et al. 2014. OPT3 Is a phloem-specific iron transporter that is essential for systemic iron signaling and redistribution of iron and cadmium in Arabidopsis. Plant Cell 26: 2249-2264.