EMRE AKSOY, Bayram Ali YERLİKAYA, Sefa AYTEN, Buasimuhan ABUDUREYİMU

Bitkilerde Rizosferden Demir Alım Mekanizmaları

Demir, toprakta en çok bulunan elementlerden bir tanesi olmasına karşın çözünürlüğü alkali topraklarda düşüktür. Dolayısıyla bu tür topraklarda yetişen bitkiler sürekli demir eksikliği stresine maruz kalırlar. Dünyadaki tarım arazilerin üçte biri bu tür topraklardan oluştuğundan dolayı tedavi edilemeyen demir eksikliği tarımsal üretimi kısıtlar. Bitkilerde gözlenen demir eksikliğinin tedavisinde farklı demir gübreleri kullanılmaktadır. Ancak, bu gübrelerin kullanımı üretim maliyetlerini artırmaktadır. Maliyetlerin azaltılabilmesi için bitkilerin toprakta bulunan demiri en etkin biçimde kullanabilmeleri gerekir. Bunun için de ilk olarak bitkilerin topraktaki demiri nasıl kök içerisine aldıklarının incelenmesi gerekmektedir. Son otuz yılda yapılan çalışmalarda farklı bitki gruplarının 3 farklı demir alım mekanizması kullandıkları keşfedilmiştir. Bu derlemenin amacı, demirin kök içerisine alımından sorumlu taşıyıcılar ile bu taşıyıcılar hakkındaki güncel gelişmelerden bahsetmektir.

Iron Uptake Mechanisms from the Rhizosphere in Plants

Solubility of iron is limited in calcareous soil although it is one of the most common elements in earth’s crust. Therefore, plants growing in this kind of soil are constantly exposed to the stress of iron deficiency. When untreated, iron deficiency restricts agricultural production because one third of the agricultural land in the world is made up of this type of soil. Different iron fertilizers are used in the treatment of iron deficiency observed in plants. However, the use of these fertilizers increases production costs. In order to reduce the cost, plants must be able to use the most effective way to extract iron from the soil. For this reason, it is necessary to first examine how the plants take iron into roots from the soil. It has been discovered that during the last three decades, different plant groups used three different iron uptake mechanisms. The purpose of this review is to talk about the transporters responsible for the uptake of iron into the root, and the current developments about these transporters.

PDF

___

Amir R, Hacham Y, Galili G. 2002. Cystathionine γ-synthase and threonine synthase operate in concert to regulate carbon flow towards methionine in plants. Trends in Plant Science 7: 153-156.
Anjum NA, Umar S, Singh S, Nazar R, Khan NA. 2008. Sulfur assimilation and cadmium tolerance in plants. In Sulfur assimilation and abiotic stress in plants. Springer. Netherlands. pp. 271-302.
Aoyama T, Kobayashi T, Takahashi M, Nagasaka S, Usuda K, Kakei Y, Ishimaru Y, Nakanishi H, Mori S, Nishizawa NK. 2009. OsYSL18 is a rice iron (III)–deoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints. Plant Molecular Biology 70: 681- 692.
Bashir K, Inoue H, Nagasaka S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK. 2006. Cloning and characterization of deoxymugineic acid synthase genes from graminaceous plants. Journal of Biological Chemistry 281: 32395-32402.
Blair MW, Knewtson SJ, Astudillo C, Li CM, Fernandez AC, Grusak MA. 2010. Variation and inheritance of iron reductase activity in the roots of common bean (Phaseolus vulgaris L.) and association with seed iron accumulation QTL. BMC Plant Biology 10(1): 215.
Buckhout TJ, Yang TJ, Schmidt W. 2009. Early iron-deficiencyinduced transcriptional changes in Arabidopsis roots as revealed by microarray analyses. BMC Genomics. 10: 147.
Cheng L, Wang F, Shou H, Huang F, Zheng L, He F, Li J, Zhao F-J, Ueno D, Ma JF. 2007. Mutation in nicotianamine aminotransferase stimulated the Fe (II) acquisition system and led to iron accumulation in rice. Plant Physiology 145: 1647-1657.
Colangelo EP, Guerinot ML. 2004. The essential basic helixloop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16: 3400-3412.
Connolly EL, Campbell NH, Grotz N, Prichard CL, Guerinot ML. 2003. Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiology 133: 1102-1110.
Connolly EL, Fett JP, Guerinot ML. 2002. Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14: 1347- 1357.
Conte SS, Walker EL. 2011. Transporters contributing to iron trafficking in plants. Molecular Plant 4: 464-476.
Curie C, Cassin G, Couch D, Divol F, Higuchi K, Jean M, Misson J, Schikora A, Czernic P, Mari S. 2009. Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Annals of Botany 103: 1-11.
Curie C, Mari S. 2017. New routes for plant iron mining. New Phytologist 214(2): 521-525.
Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Brait JF, Walker EL. 2001. Maize yellow stripe1 encodes a membrane protein directly involved in Fe3+ uptake. Nature 409:346–349.
Driessen P, Deckers J, Spaargaren O, Nachtergaele F. 2000. Lecture notes on the major soils of the world. Food and Agriculture Organization (FAO).
Eide D, Broderius M, Fett J, Guerinot ML. 1996. A novel ironregulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci U S A 93: 5624-5628.
Feng H, An F, Zhang S, Ji Z, Ling H-Q, Zuo J. 2006. Lightregulated, tissue-specific, and cell differentiation-specific expression of the Arabidopsis Fe (III)-chelate reductase gene AtFRO6. Plant Physiology 140: 1345-1354.
Gonzalez-Vallejo EB, Susın S, Abadıa A, Abadıa J. 1998. Changes in sugar beet leaf plasma membrane Fe(III)-chelate reductase activities mediated by Fedeficiency, assay buffer composition, anaerobiosis and the presence of flavins. Protoplasma 205: 163–168.
Gross J, Stein RJ, Fett-Neto AG, Fett JP. 2003. Iron homeostasis related genes in rice. Genetics and Molecular Biology 26: 477-497.
Grotz N, Guerinot ML. 2006. Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochimica Et Biophysica ActaMolecular Cell Research 1763: 595-608.
Grusak MA, Welch RM, Kochian LV. 1990. Physiological characterization of a single-gene mutant of Pisum sativum exhibiting excess iron accumulation I. Root iron reduction and iron uptake. Plant Physiology 93(3): 976-981.
Guerinot ML. 2010. Iron. In R Hell, R-R Mendel, eds, Cell Biology of Metals and Nutrients. Springer Science. pp 75- 94.
Fourcroy P, Sisó‐Terraza P, Sudre D, Savirón M, Reyt G, Gaymard F, Abadía A, Abadia J, Álvarez‐Fernández A, Briat JF. 2014. Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytologist 201(1): 155- 167.
Fourcroy P, Tissot N, Gaymard F, Briat JF, Dubos C. 2016. Facilitated Fe nutrition by phenolic compounds excreted by the Arabidopsis ABCG37/PDR9 transporter requires the IRT1/FRO2 high-affinity root Fe2+ transport system. Molecular Plant 9(3): 485-488.
Haydon MJ, Cobbett CS. 2007. A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis. Plant Physiology 143(4): 1705-1719.
Haydon MJ, Kawachi M, Wirtz M, Hillmer S, Hell R, Krämer U. 2012. Vacuolar nicotianamine has critical and distinct roles under iron deficiency and for zinc sequestration in Arabidopsis. The Plant Cell 24(2): 724-737.
Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J, Millar AH. 2004. Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. The Plant Cell 16: 241-256.
Hell R, Stephan UW. 2003. Iron uptake, trafficking and homeostasis in plants. Planta 216: 541-551.
Henriques R, Jasik J, Klein M, Martinoia E, Feller U, Schell J, Pais MS, Koncz C. 2002. Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Molecular Biology 50: 587-597.
Higa A, Mori Y, Kitamura Y. 2010. Iron deficiency induces changes in riboflavin secretion and the mitochondrial electron transport chain in hairy roots of Hyoscyamus albus. Journal of Plant Physiology 167: 870–878.
Higuchi K, Suzuki K, Nakanishi H, Yamaguchi H, Nishizawa N-K, Mori S. 1999. Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiology 119: 471-480.
Higuchi K, Watanabe S, Takahashi M, Kawasaki S, Nakanishi H, Nishizawa NK, Mori S. 2001. Nicotianamine synthase gene expression differs in barley and rice under Fe‐deficient conditions. The Plant Journal 25(2): 159-167.
Inoue H, Higuchi K, Takahashi M, Nakanishi H, Mori S, Nishizawa NK. 2003. Three rice nicotianamine synthase genes, OsNAS1, OsNAS2, and OsNAS3 are expressed in cells involved in long‐distance transport of iron and differentially regulated by iron. The Plant Journal 36(3): 366-381.
Inoue H, Takahashi M, Kobayashi T, Suzuki M, Nakanishi H, Mori S, Nishizawa NK. 2008. Identification and localization of rice nicotianamine aminotransferase OsNAAT1 expression suggests the site of phytosiderophore synthesis in rice. Plant Mol. Biol. 66: 193–203.
Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa NK. 2009. Rice OsYSL15 is an iron-regulated iron (III)- deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. Journal of Biological Chemistry 284: 3470-3479.
Ishimaru Y, Kakei Y, Shimo H, Bashir K, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK. 2011. A rice phenolic efflux transporter is essential for solubilizing precipitated apoplasmic iron in the plant stele. Journal of Biological Chemistry 286(28): 24649-24655.
Ishimaru Y, Kim S, Tsukamoto T, Oki H, Kobayashi T, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S. 2007. Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil. Proceedings of the National Academy of Sciences. 104: 7373-7378.
Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, Wada Y, Watanabe S, Matsuhashi S, Takahashi M. 2006. Rice plants take up iron as an Fe3+‐ phytosiderophore and as Fe2+. The Plant Journal. 45: 335- 346.
Itai R, Suzuki K, Yamaguchi H, Nakanishi H, Nishizawa NK, Yoshimura E, Mori S. 2000. Induced activity of adenine phosphoribosyltransferase (APRT) in iron‐deficient barley roots: a possible role for phytosiderophore production. Journal of Experimental Botany. 51: 1179-1188.
Ivanov R, Brumbarova T, Bauer P. 2012. Fitting into the harsh reality: regulation of iron-deficiency responses in dicotyledonous plants. Molecular Plant. 5: 27-42.
Jakoby M, Wang HY, Reidt W, Weisshaar B, Bauer P. 2004. FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS Letters. 577: 528-534.
Jeong J, Cohu C, Kerkeb L, Pilon M, Connolly EL, Guerinot ML. 2008. Chloroplast Fe (III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proceedings of the National Academy of Sciences. 105: 10619-10624.
Jeong J, Connolly EL. 2009. Iron uptake mechanisms in plants: Functions of the FRO family of ferric reductases. Plant Science. 176: 709-714.
Jin CW, Ye YQ, Zheng, SJ. 2014. An under ground tale:contribution of microbial activity to plant iron acquisition via ecological processes. Annanls of Botany 113: 7–18. doi:10.1093/aob/mct249.
Jordan CM, Wakeman RJ, Devay JE. 1992. Toxicity of free riboflavin and methionine-riboflavin solutions to Phytophthora infestans and the reduction of potato late blight disease. Canadian Journal of Microbiology. 38: 1108– 1111.
Kakei Y, Ishimaru Y, Kobayashi T, Yamakawa T, Nakanishi H, Nishizawa NK. 2012. OsYSL16 plays a role in the allocation of iron. Plant molecular Biology 79(6): 583-594.
Kim SA, Guerinot ML. 2007. Mining iron: Iron uptake and transport in plants. Febs Letters. 581: 2273-2280.
Klatte M, Schuler M, Wirtz M, Fink-Straube C, Hell R, Bauer P. 2009. The Analysis of Arabidopsis Nicotianamine Synthase Mutants Reveals Functions for Nicotianamine in Seed Iron Loading and Iron Deficiency Responses. Plant Physiology. 150: 257-271.
Klein MA, López-Millán AF, Grusak MA. 2012. Quantitative trait locus analysis of root ferric reductase activity and leaf chlorosis in the model legume, Lotus japonicus. Plant and Soil 351(1-2): 363-376.
Kobayashi T, Nakanishi H, Nishizawa NK. 2010. Recent insights into iron homeostasis and their application in graminaceous crops. Proceedings of the Japan Academy Series B-Physical and Biological Sciences. 86: 900-913.
Kobayashi T, Nakanishi H, Takahashi M, Kawasaki S, Nishizawa N-K, Mori S. 2001. In vivo evidence that Ids3 from Hordeum vulgare encodes a dioxygenase that converts 2′-deoxymugineic acid to mugineic acid in transgenic rice. Planta. 212: 864-871.
Kobayashi T, Nishizawa NK. 2012. Iron uptake, translocation, and regulation in higher plants. Annual Review of Plant Biology. 63: 131-152.
Kobayashi T, Suzuki M, Inoue H, Itai RN, Takahashi M, Nakanishi H, Mori S, Nishizawa NK. 2005. Expression of iron-acquisition-related genes in iron-deficient rice is coordinately induced by partially conserved iron-deficiencyresponsive elements. Journal of Experimental Botany. 56: 1305-1316.
Kobayashi T, Itai RN, Nishizawa NK. 2014. Iron deficiency responses in rice roots. Rice 7:27.
Koike S, Inoue H, Mizuno D, Takahashi M, Nakanishi H, Mori S, Nishizawa NK. 2004. OsYSL2 is a rice metal‐ nicotianamine transporter that is regulated by iron and expressed in the phloem. The Plant Journal. 39: 415-424.
Lan P, Li WF, Wen TN, Schmidt W. 2012. Quantitative phosphoproteome profiling of iron-deficient Arabidopsis roots. Plant Physiology 159: 403–417.
Li L, Cheng X, Ling H-Q. 2004. Isolation and characterization of Fe (III)-chelate reductase gene LeFRO1 in tomato. Plant Molecular Biology. 54: 125-136.
Li W, Santi S, Tan C, W. S. 2007. Dissecting P-type H+- ATPase-mediated proton extrusion in Arabidopsis. In 18th International Conference on Arabidopsis Research. Beijing, China.
Li S, Zhou X, Huang Y, Zhu L, Zhang S, Zhao Y, Guo J, Chen J, Chen R. 2013. Identification and characterization of the zinc-regulated transporters, iron-regulated transporter-like protein (ZIP) gene family in maize. BMC Plant Biol. 13:114.
Li S, Zhou X, Li H, Liu Y, Zhu L, Guo J, Liu X, Fan Y, Chen J, Chen RR. 2015. Overexpression of ZmIRT1 and ZmZIP3 enhances iron and zinc accumulation in transgenic Arabidopsis. PloS One 10(8): e0136647.
Li S, Zhou X, Chen J, Chen R. 2016. Is there a strategy I iron uptake mechanism in maize? Plant Signaling and Behavior http://dx.doi.org/10.1080/15592324.2016.1161877
Lopez-Millan AF, Morales F, Andaluz S, Gogorcena Y, Abadıa A, De Las Rivas J, Abadia J. 2000. Responses of sugar beet roots to iron deficiency. Changes in carbon assimilation and oxygen use. Plant Physiology. 124: 885–897.
Ma JF, Taketa S, Chang YC, Iwashita T, Matsumoto H, Takeda K, Nomoto K. 1999. Genes controlling hydroxylations of phytosiderophores are located on different chromosomes in barley (Hordeum vulgare L.). Planta 207(4): pp.590-596.
Marschner H. 1995. Mineral nutrition of higher plants. London, UK:AcademicPress.
Marschner H, Marschner P. 2011. Marschner's mineral nutrition of higher plants, Vol 89. Elsevier. Marschner H, Romheld V. 1994. Strategies of plants for acquisition of iron. Plant and Soil. 165: 261-274.
Mizuno D, Higuchi K, Sakamoto T, Nakanishi H, Mori S, Nishizawa NK. 2003. Three nicotianamine synthase genes isolated from maize are differentially regulated by iron nutritional status. Plant Physiology 132(4): 1989-1997.
Mori S, Nishizawa N. 1987. Methionine as a dominant precursor of phytosiderophores in Graminaceae plants. Plant Cell Physiol. 28:1081–92.
Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, BLÄSING O, Usadel B, Czechowski T, Udvardi MK, Stitt M, Scheible WR. 2007. Genome‐wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant, Cell & Environment 30(1): 85-112.
Mukherjee I, Campbell NH, Ash JS, Connolly EL. 2006. Expression profiling of the Arabidopsis ferric chelate reductase (FRO) gene family reveals differential regulation by iron and copper. Planta 223: 1178-1190 Plant, Cell & Environment. 30: 85–112.
Murata Y, Ma JF, Yamaji N, Ueno D, Nomoto K, Iwashita T. 2006. A specific transporter for iron (III)–phytosiderophore in barley roots. The Plant Journal. 46: 563-572.
Nagasaka S, Takahashi M, Nakanishi-Itai R, Bashir K, Nakanishi H, Mori S, Nishizawa NK. 2009. Time course analysis of gene expression over 24 hours in Fe-deficient barley roots. Plant Molecular Biology. 69: 621-631.
Nakanishi H, Yamaguchi H, Sasakuma T, Nishizawa NK, Mori S. 2000. Two dioxygenase genes, Ids3 and Ids2, from Hordeum vulgare are involved in the biosynthesis of mugineic acid family phytosiderophores. Plant Molecular Biology. 44: 199-207.
Nozoye T, Itai RN, Nagasaka S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK. 2004. Diurnal changes in the expression of genes that participate in phytosiderophore synthesis in rice. Soil Science and Plant Nutrition 50(7): 1125-1131.
Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK. 2011. Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. Journal of Biological Chemistry 286(7): 5446-5454.
Nozoye T, Nagasaka S, Kobayashi T, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK. 2015. The phytosiderophore efflux transporter TOM2 is involved in metal transport in rice. Journal of Biological Chemistry 290(46): 27688-27699.
Oki H, Kim S, Nakanishi H, Takahashi M, Yamaguchi H, Mori S, Nishizawa NK. 2004. Directed evolution of yeast ferric reductase to produce plants with tolerance to iron deficiency in alkaline soils. Soil Science and Plant Nutrition. 50: 1159- 1165.
Palmer CM, Guerinot ML. 2009. Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat Chem Biol. 5: 333-340.
Pao SS, Paulsen IT, Saier MH. 1998. Major facilitator superfamily. Microbiology and Molecular Biology Reviews 62(1): 1-34.
Puig S, Andres-Colas N, Garcia-Molina A, Penarrubia L. 2007. Copper and iron homeostasis in Arabidopsis: responses to metal deficiencies, interactions and biotechnological applications. Plant Cell and Environment. 30: 271-290.
Ravanel S, Droux M, Douce R. 1995. Methionine Biosynthesis in Higher-Plants. 1. Purification and Characterization of Cystathionine γ-Synthase from Spinach Chloroplasts. Archives of Biochemistry And Biophysics. 316: 572-584.
Rellan-Alvarez R, Giner-Martinez-Sierra J, Orduna J, Orera I, Rodriguez-Castrillon JA, Garcia-Alonso JI, Abadia J, Alvarez-Fernandez A. 2010. Identification of a tri-iron(III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron longdistance transport. Plant Cell Physiol. 51: 91-102.
Rellán-Álvarez R, Andaluz,S, Rodríguez-Celma J, Wohlgemuth G, Zocchi G, Álvarez-Fernández A, Fiehn O, López-Millán AF, Abadía J. 2010. Changes in the proteomic and metabolic profiles of Beta vulgaris root tips in response to iron deficiency and resupply. BMC Plant Biology 10(1): 120.
Robinson NJ, Procter CM, Connolly EL, Guerinot ML. 1999. A ferric-chelate reductase for iron uptake from soils. Nature. 397: 694-697.
Rodríguez-Celma J. 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.
Rodriguez-Celma J, Lattanzio G, Grusak MA, Abadıa A, Abadıa J, Lopez-Millan AF. 2011a. Root responses of Medicago truncatula plants grown in two different iron deficiency conditions: changes in root protein profile and riboflavin biosynthesis. Journal of Proteome Research. 10: 2590–2601.
Rodriguez-Celma J, Vazquez-Reina S, Orduna J, Abadia A, Abadia J, Alvarez-Fernandez A, Lopez-Millan AF. 2011b. Characterization of flavins in roots of Fe-deficient Strategy I plants, with a focus on Medicago truncatula. Plant and Cell Physiology. 52: 2173–2189.
Rodriguez-Celma J, Lin WD, Fu GM, Abadia J, Lopez-Millan 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.
Romheld V. 1987. Different strategies for iron acquisition in higher-plants. Physiologia Plantarum. 70: 231-234.
Romheld V, Marschner H. 1983. Mechanism of iron uptake by peanut plants. I. FeIII reduction, chelate splitting, and release of phenolics. Plant Physiology. 71: 949–954.
Santi S, Schmidt W. 2009. Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol. 183: 1072-1084.
Schaaf G, Ludewig U, Erenoglu BE, Mori S, Kitahara T, von Wirén N. 2004. ZmYS1 functions as a protoncoupled symporter for phytosiderophore-and nicotianaminechelated metals. Journal of Biological Chemistry 279(10): 9091- 9096.
Schagerlöf U, Wilson G, Hebert H, Al-Karadaghi S, Hägerhäll C. 2006. Transmembrane topology of FRO2, a ferric chelate reductase from Arabidopsis thaliana. Plant Molecular Biolog.y 62: 215-221.
Schmid NB, Giehl RF, Döll S, Mock HP, Strehmel N, Scheel D, Kong X, Hider RC, von Wirén N. 2014. Feruloyl-CoA 6′- hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis. Plant Physiology 164(1): 160-172
Schmidt W. 1999. Mechanisms and regulation of reductionbased iron uptake in plants. New Phytologist. 141: 1-26.
Schmidt W, Buckhout TJ. 2011. A hitchhiker's guide to the Arabidopsis ferrome. Plant Physiol Biochem. 49: 462-470.
Schmidt H, Günther C, Weber M, Spörlein C, Loscher S, Böttcher C, Schobert R, Clemens S. 2014. Metabolome analysis of Arabidopsis thaliana roots identifies a key metabolic pathway for iron acquisition. PLoS One 9(7): e102444.
Schmiedeberg L, Krüger C, Stephan UW, Bäumlein H, Hell R. 2003. Synthesis and proof‐of‐function of a [14C]‐labelled form of the plant iron chelator nicotianamine using recombinant nicotianamine synthase from barley. Physiologia Plantarum 118(3): 430-438.
Scholz G, Becker R, Pich A, Stephan UW. 1992. Nicotianamine‐a common constituent of strategies I and II of iron acquisition by plants: A review. Journal of Plant Nutrition 15(10): 1647-1665.
Shojima S, Nishizawa NK, Fushiya S, Nozoe S, Irifune T, Mori S. 1990. Biosynthesis of phytosiderophores: in vitro biosynthesis of 2 -deoxymugineic acid from L-methionine and nicotianamine. Plant Physiol. 93:1497–503.
Sisó‐Terraza P, Rios JJ, Abadía J, Abadía A, Álvarez‐Fernández A. 2016. Flavins secreted by roots of iron‐deficient Beta vulgaris enable mining of ferric oxide via reductive mechanisms. New Phytologist 209(2): 733-745.
Susin S, Abian J, Sanchez-Baeza F, Peleato ML, Abadia A, Gelpi E, Abadia J. 1993. Riboflavin 30- and 50-sulfate, two novel flavins accumulating in the roots of iron-deficient sugar-beet (Beta vulgaris). Journal of Biological Chemistry. 268: 20 958–20 965.
Susin S, Abian J, Peleato ML, Sanchez-Baeza F, Abadıi A, Gelpı E, Abadia J. 1994. Flavin excretion from roots of irondeficient sugar beet (Beta vulgaris L.). Planta. 193: 514– 519.
Suzuki M, Nozoye T, Nagasaka S, Nakanishi H, Nishizawa NK, Mori S. 2016. The detection of endogenous 2’- deoxymugineic acid in olives (Olea europaea L.) indicates the biosynthesis of mugineic acid family phytosiderophores in non-graminaceous plants. Soil Science and Plant Nutrition 62(5-6): 481-488.
Takagi S. 1976. Naturally occurring iron-chelating compounds in oat-and rice-root washings: I. Activity Measurement and Preliminary Characterization. Soil Science And Plant Nutrition 22: 423-433.
Takagi Si, Nomoto K, Takemoto T. 1984. Physiological aspect of mugineic acid, a possible phytosiderophore of graminaceous plants. Journal of Plant Nutrition. 7: 469-477.
Takahashi M, Yamaguchi H, Nakanishi H, Shioiri T, Nishizawa N-K, Mori S. 1999. Cloning two genes for nicotianamine aminotransferase, a critical enzyme in iron acquisition (Strategy II) in graminaceous plants. Plant Physiology. 121: 947-956.
Takahashi M, Terda Y, Nakai I, Nakanishi H, Yoshimura E, Mori S, Nishikawa NK. 2003. Role of nicotianamine in the itracellular delivery of metals and plant reproductive devolopment. Plant Cell. 15:1263–1280.
Thomine S, Lanquar V. 2011. Iron Transport and Signaling in Plants. In Transporters and Pumps in Plant Signaling: 99-131.
Thomine S, Vert G. 2013. Iron transport in plants: better be safe than sorry. Current Opinion in Plant Biology 16(3): 322-327
Tsai HH, Schmidt W. 2017. One way. Or another? Iron uptake in plants. New Phytologist 214(2): 500-505.
Ueno D, Rombola AD, Iwashita T, Nomoto K, Ma JF. 2007. Identification of two new phytosiderophores secreted by perennial grasses. New Phytol. 174:304–310.
Varotto C, Maiwald D, Pesaresi P, Jahns P, Salamini F, Leister D. 2002. The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant Journal. 31: 589-599.
Vasconcelos M, Eckert H, Arahana V, Graef G, Grusak MA, Clemente T. 2006. Molecular and phenotypic characterization of transgenic soybean expressing the Arabidopsis ferric chelate reductase gene, FRO2. Planta. 224: 1116-1128.
Vert G, Barberon M, Zelazny E, Seguela M, Briat JF, Curie C. 2009. Arabidopsis IRT2 cooperates with the high-affinity iron uptake system to maintain iron homeostasis in root epidermal cells. Planta. 229: 1171-1179.
Vert G, Briat JF, Curie C. 2001. Arabidopsis IRT2 gene encodes a root‐periphery iron transporter. The Plant Journal. 26: 181- 189.
Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF, Curie C. 2002. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell. 14: 1223-1233.
Waters BM, Blevins DG, Eide DJ. 2002. Characterization of FRO1, a pea ferric-chelate reductase involved in root iron acquisition. Plant Physiology. 129: 85-94.
Waters BM, Lucena C, Romera FJ, Jester GG, Wynn AN, Rojas CL, Alcantara E, Perez-Vicente R. 2007. Ethylene involvement in the regulation of the H+-ATPase CsHA1 gene and of the new isolated ferric reductase CsFRO1 and iron transporter CsIRT1 genes in cucumber plants. Plant Physiology and Biochemistry. 45: 293-301.
Weber G, von Wrien N, Hayen H. 2008. Investigation of ascoebate-mediated iron release from ferric phytosiderophores in the presence of nicotianamine. Biometals. 21:503–513.
Welch RM. 1995. Micronutrient Nutrition of Plants. Critical Reviews in Plant Sciences. 14: 49-82.
Welkie GW. 2000. Taxonomic distribution of dicotyledonous species capable of root excretion of riboflavin under iron deficiency. Journal of Plant Nutrition. 23: 1819–1831.
White JP. 2012. Ion Uptake Mechanisms of Individual Cells and Roots: Short-distance Transport. In Marschner's Mineral Nutrition of Higher Plants, Ed 3rd. Academic Press, London; Waltham, MA, pp 7-47.
White PJ, Brown PH. 2010 Plant nutrition for sustainable development and global health. Annals of Botany. 105: 1073-1080.
Wu H, Li L, Du J, Yuan Y, Cheng X, Ling H-Q. 2005. Molecular and biochemical characterization of the Fe (III) chelate reductase gene family in Arabidopsis thaliana. Plant and Cell Physiology. 46: 1505-1514.
Yi Y, Guerinot ML. 1996. Genetic evidence that induction of root Fe(III) chelate reductase activity is necessary for iron uptake under iron deficiency. Plant Journal. 10: 835-844.
Zamioudis C, Hanson J, Pieterse CM. 2014. β‐Glucosidase BGLU42 is a MYB72‐dependent key regulator of rhizobacteria‐induced systemic resistance and modulates iron deficiency responses in Arabidopsis roots. New Phytologist 204(2): 368-379.
Zheng L, Yamaji N, Yokosho K, Ma JF. 2012. YSL16 is a phloem-localized transporter of the copper-nicotianamine complex that is responsible for copper distribution in rice. The Plant Cell 24(9): 3767-3782.
Ziegler J, Schmidt S, Chutia R, M€uller J, B€ottcher C, Strehmel N, Scheel D, Abel S. 2016. Non-targeted profiling of semi-polar metabolites in Arabidopsis root exudates uncovers a role for coumarin secretion and lignification during the local response to phosphate limitation. Journal of Experimental Botany. 67: 1421–1432.