Evaluation of constitutive iron reductase (AtFRO2) expression on mineral accumulation and distribution in soybean (Glycine max. L)

Iron is an important micronutrient in human and plant nutrition. Adequate iron nutrition during crop production is central for assuring appropriate iron concentrations in the harvestable organs, for human food or animal feed. The whole-plant movement of iron involves several processes, including the...

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Published inFrontiers in plant science Vol. 5; p. 112
Main Authors Vasconcelos, Marta W, Clemente, Thomas E, Grusak, Michael A
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 03.04.2014
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Abstract Iron is an important micronutrient in human and plant nutrition. Adequate iron nutrition during crop production is central for assuring appropriate iron concentrations in the harvestable organs, for human food or animal feed. The whole-plant movement of iron involves several processes, including the reduction of ferric to ferrous iron at several locations throughout the plant, prior to transmembrane trafficking of ferrous iron. In this study, soybean plants that constitutively expressed the AtFRO2 iron reductase gene were analyzed for leaf iron reductase activity, as well as the effect of this transgene's expression on root, leaf, pod wall, and seed mineral concentrations. High Fe supply, in combination with the constitutive expression of AtFRO2, resulted in significantly higher concentrations of different minerals in roots (K, P, Zn, Ca, Ni, Mg, and Mo), pod walls (Fe, K, P, Cu, and Ni), leaves (Fe, P, Cu, Ca, Ni, and Mg) and seeds (Fe, Zn, Cu, and Ni). Leaf and pod wall iron concentrations increased as much as 500% in transgenic plants, while seed iron concentrations only increased by 10%, suggesting that factors other than leaf and pod wall reductase activity were limiting the translocation of iron to seeds. Protoplasts isolated from transgenic leaves had three-fold higher reductase activity than controls. Expression levels of the iron storage protein, ferritin, were higher in the transgenic leaves than in wild-type, suggesting that the excess iron may be stored as ferritin in the leaves and therefore unavailable for phloem loading and delivery to the seeds. Also, citrate and malate levels in the roots and leaves of transgenic plants were significantly higher than in wild-type, suggesting that organic acid production could be related to the increased accumulation of minerals in roots, leaves, and pod walls, but not in the seeds. All together, these results suggest a more ubiquitous role for the iron reductase in whole-plant mineral accumulation and distribution.
AbstractList Iron is an important micronutrient in human and plant nutrition. Adequate iron nutrition during crop production is central for assuring appropriate iron concentrations in the harvestable organs, for human food or animal feed. The whole-plant movement of iron involves several processes, including the reduction of ferric to ferrous iron at several locations throughout the plant, prior to transmembrane trafficking of ferrous iron. In this study, soybean plants that constitutively expressed the AtFRO2 iron reductase gene were analyzed for leaf iron reductase activity, as well as the effect of this transgene's expression on root, leaf, pod wall, and seed mineral concentrations. High Fe supply, in combination with the constitutive expression of AtFRO2, resulted in significantly higher concentrations of different minerals in roots (K, P, Zn, Ca, Ni, Mg and Mo), pod walls (Fe, K, P, Cu and Ni), leaves (Fe, P, Cu, Ca, Ni and Mg) and seeds (Fe, Zn, Cu and Ni). Leaf and pod wall iron concentrations increased as much as 500% in transgenic plants, while seed iron concentrations only increased by 10%, suggesting that factors other than leaf and pod wall reductase activity were limiting the translocation of iron to seeds. Protoplasts isolated from transgenic leaves had three-fold higher reductase activity than controls. Expression levels of the iron storage protein, ferritin, were higher in the transgenic leaves than in wild-type, suggesting that the excess iron may be stored as ferritin in the leaves and therefore unavailable for phloem loading and delivery to the seeds. Also, citrate and malate levels in the roots and leaves of transgenic plants were significantly higher than in wild-type, suggesting that organic acid production could be related to the increased accumulation of minerals in roots, leaves and pod walls, but not in the seeds. All together, these results suggest a more ubiquitous role for the iron reductase in whole-plant mineral accumulation and distribution.
Author Grusak, Michael A
Vasconcelos, Marta W
Clemente, Thomas E
AuthorAffiliation 1 Centro de Biotecnologia e Química Fina, Escola Superior de Biotecnologia, Centro Regional do Porto da Universidade Católica Portuguesa Porto, Portugal
3 Center for Biotechnology – Plant Science Initiative, University of Nebraska-Lincoln Lincoln, NE, USA
2 Department of Pediatrics, USDA-ARS Children’s Nutrition Research Center, Baylor College of Medicine Houston, TX, USA
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  organization: Centro de Biotecnologia e Química Fina, Escola Superior de Biotecnologia, Centro Regional do Porto da Universidade Católica Portuguesa Porto, Portugal ; Department of Pediatrics, USDA-ARS Children's Nutrition Research Center, Baylor College of Medicine Houston, TX, USA
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Cites_doi 10.1046/j.1365-313X.2003.01760.x
10.1007/s11103-006-9015-0
10.1111/jipb.12041
10.1111/j.1469-8137.2012.04167.x
10.1104/pp.124.2.885
10.1093/oxfordjournals.aob.a085415
10.1016/j.jplph.2008.06.011
10.1007/BF00009935
10.1104/pp.113.220426
10.1016/j.pbi.2011.03.025
10.1016/j.foodres.2012.12.021
10.1016/j.jplph.2009.09.007
10.1186/1939-8433-5-27
10.1093/aob/mcn207
10.1007/BF00239946
10.1016/j.bbamcr.2012.03.010
10.1007/s11627-001-0123-x
10.1104/pp.98.3.1128
10.1186/1471-2229-11-152
10.1007/s00425-006-0293-1
10.1104/pp.93.2.723
10.1023/A:1026438615520
10.1016/S0176-1617(11)82052-3
10.1093/pcp/pce012
10.1021/bi901573b
10.1111/j.1469-8137.2007.02288.x
10.1046/j.1365-313X.1996.10050835.x
10.1016/S0044-328X(82)80038-X
10.1016/S0015-3796(89)80080-0
10.1080/01904169009364070
10.1146/annurev.arplant.54.031902.135018
10.1104/pp.122.2.337
10.1074/jbc.M105392200
10.1007/BF00196606
10.1104/pp.104.2.649
10.1023/B:PLAN.0000038271.96019.aa
10.1007/s00425-002-0920-4
10.1093/pcp/pcp170
10.1073/pnas.93.11.5624
10.1104/pp.103.025122
10.1111/j.1469-8137.2008.02738.x
10.1111/j.1365-313X.2010.04158.x
10.1017/S0960258500004293
10.1104/pp.80.1.175
10.1104/pp.41.3.510
10.1105/tpc.001388
10.1111/j.1399-3054.1975.tb03780.x
10.1146/annurev-arplant-042811-105522
10.1093/mp/ssr065
10.1111/nph.12471
10.1007/s00425-005-0165-0
10.1038/17800
10.1104/pp.48.3.273
10.1093/jxb/47.5.669
10.1104/pp.105.074138
10.1023/A:1016093317898
10.1073/pnas.0708367105
10.1111/j.1365-313X.2004.02146.x
10.1038/srep00543
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Copyright Copyright © 2014 Vasconcelos, Clemente and Grusak. 2014
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Keywords soybean
iron
transgenic
FRO2
mineral nutrition
Language English
License This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
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Reviewed by: Sebastien Thomine, Centre National de la Recherche Scientifique, France; Graziano Zocchi, Università degli Studi di Milano, Italy
Edited by: Paloma Koprovski Menguer, John Innes Centre, UK
Present address: Marta W. Vasconcelos, Laboratório Associado, Centro de Biotecnologia e Química Fina, Escola Superior de Biotecnologia, Universidade Católica do Porto, Rua Dr. António Bernardino de Almeida, 4200-072 Porto, Portugal
This article was submitted to Plant Nutrition, a section of the journal Frontiers in Plant Science.
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References Masuda (B38) 2012; 2
Stephan (B48) 1989; 185
López-Millán (B31) 2000; 124
Tiffin (B50) 1966; 41
Abadía (B1) 2002; 241
Grusak (B16) 1995; 197
Thomine (B49) 2003; 34
Schagerlof (B46) 2006; 62
Tiffin (B51) 1971; 48
López-Millán (B30) 2004; 54
Römheld (B45) 1986; 80
Fourcroy (B13) 2013; 201
Kobayashi (B23) 2012; 63
Mukherjee (B39) 2006; 223
Eide (B11) 1996; 93
Majumder (B34) 1990; 123
Waters (B56) 2008; 177
Jeong (B22) 2008; 105
Zhang (B60) 1995; 146
Curie (B6) 2003; 54
Rellán-álvarez (B41) 2010; 51
Lucas (B33) 2013; 55
Ivanov (B21) 2012; 5
Sperotto (B47) 2012; 5
Dwiyanti (B10) 2011; 11
Vasconcelos (B53) 2006; 224
Hindt (B19) 2012; 1823
Truty (B52) 2001; 276
Larbi (B27) 2010; 167
Kochian (B24) 1991
Lazlo (B29) 1990; 13
Grusak (B15) 1994; 104
Koike (B25) 2004; 39
Brüggemann (B2) 1993; 190
Curie (B7) 2009; 103
Robinson (B43) 1999; 397
Marschner (B37) 1982; 105
Marschner (B36) 1995
Gonzalez-Vallejo (B14) 2000; 122
Zeng (B61) 2005; 12
Feng (B12) 2006; 140
Yi (B59) 1996; 10
Marentes (B35) 1998; 8
Ramani (B40) 1987; 33
Zimmermann (B62) 2009; 48
Carvalho (B4) 2013; 54
Hell (B17) 2003; 216
Rodríguez-Celma (B44) 2013; 162
Welch (B57) 1990; 93
Walker (B55) 2011; 14
Hocking (B18) 1977; 41
Ishimaru (B20) 2010; 62
Connolly (B3) 2003; 133
de la Guardia (B8) 1996; 47
López-Millán (B32) 2009; 66
Remy (B42) 2012; 195
Dinkins (B9) 2001; 37
White (B58) 2009; 182
Larbi (B28) 2001; 42
Korshunova (B26) 1999; 40
Vert (B54) 2002; 14
Crafts-Brandner (B5) 1992; 98
References_xml – volume: 34
  start-page: 685
  year: 2003
  ident: B49
  article-title: AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency.
  publication-title: Plant J.
  doi: 10.1046/j.1365-313X.2003.01760.x
  contributor:
    fullname: Thomine
– volume: 62
  start-page: 215
  year: 2006
  ident: B46
  article-title: Transmembrane topology of FRO2, a ferric chelate reductase from Arabidopsis thaliana.
  publication-title: Plant Mol. Biol.
  doi: 10.1007/s11103-006-9015-0
  contributor:
    fullname: Schagerlof
– volume: 55
  start-page: 294
  year: 2013
  ident: B33
  article-title: The plant vascular system: evolution, development and functions.
  publication-title: J. Integr. Plant Biol.
  doi: 10.1111/jipb.12041
  contributor:
    fullname: Lucas
– volume: 195
  start-page: 356
  year: 2012
  ident: B42
  article-title: The Pht1;9 and Pht1;8 transporters mediate inorganic phosphate acquisition by the Arabidopsis thaliana root during phosphorus starvation.
  publication-title: New Phytol.
  doi: 10.1111/j.1469-8137.2012.04167.x
  contributor:
    fullname: Remy
– volume: 124
  start-page: 885
  year: 2000
  ident: B31
  article-title: Responses of sugar beet roots to iron deficiency.Changes in carbon assimilation and oxygen use.
  publication-title: Plant Physiol.
  doi: 10.1104/pp.124.2.885
  contributor:
    fullname: López-Millán
– volume: 41
  start-page: 1259
  year: 1977
  ident: B18
  article-title: Mobilization of minerals to developing seeds of legumes.
  publication-title: Ann. Bot.
  doi: 10.1093/oxfordjournals.aob.a085415
  contributor:
    fullname: Hocking
– volume: 66
  start-page: 375
  year: 2009
  ident: B32
  article-title: Metabolic responses in iron deficient tomato plants.
  publication-title: J. Plant Physiol.
  doi: 10.1016/j.jplph.2008.06.011
  contributor:
    fullname: López-Millán
– volume: 123
  start-page: 117
  year: 1990
  ident: B34
  article-title: Genetic effect on uptake of selected nutrients in some rice (O. sativa L.) varieties in phosphorus deficient soils.
  publication-title: Plant Soil
  doi: 10.1007/BF00009935
  contributor:
    fullname: Majumder
– volume: 162
  start-page: 1473
  year: 2013
  ident: B44
  article-title: Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula.
  publication-title: Plant Physiol.
  doi: 10.1104/pp.113.220426
  contributor:
    fullname: Rodríguez-Celma
– volume: 14
  start-page: 318
  year: 2011
  ident: B55
  article-title: The role of transition metal homeostasis in plant seed development.
  publication-title: Curr. Opin. Plant Biol.
  doi: 10.1016/j.pbi.2011.03.025
  contributor:
    fullname: Walker
– volume: 54
  start-page: 961
  year: 2013
  ident: B4
  article-title: Producing more with less: ‘omics’ at the service of plant-based food biofortification.
  publication-title: Food Res. Int.
  doi: 10.1016/j.foodres.2012.12.021
  contributor:
    fullname: Carvalho
– volume: 167
  start-page: 255
  year: 2010
  ident: B27
  article-title: Changes in iron and organic acid concentrations in xylem sap and apoplastic fluid of iron-deficient Beta vulgaris plants in response to iron resupply.
  publication-title: J. Plant Physiol.
  doi: 10.1016/j.jplph.2009.09.007
  contributor:
    fullname: Larbi
– volume: 5
  start-page: 27
  year: 2012
  ident: B47
  article-title: Effects of different Fe supplies on mineral partitioning and remobilization during the reproductive development of rice (Oryza sativa L.).
  publication-title: Rice
  doi: 10.1186/1939-8433-5-27
  contributor:
    fullname: Sperotto
– volume: 103
  start-page: 1
  year: 2009
  ident: B7
  article-title: Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters.
  publication-title: Ann. Bot.
  doi: 10.1093/aob/mcn207
  contributor:
    fullname: Curie
– volume: 197
  start-page: 111
  year: 1995
  ident: B16
  article-title: Whole-root iron(III)-reductase activity throughout the life cycle of iron-grown Pisum sativum L. (Fabaceae): relevance to the iron nutrition of developing seeds.
  publication-title: Planta
  doi: 10.1007/BF00239946
  contributor:
    fullname: Grusak
– volume: 1823
  start-page: 1521
  year: 2012
  ident: B19
  article-title: Getting a sense for signals: regulation of the plant iron deficiency response.
  publication-title: Biochim. Biophys. Acta
  doi: 10.1016/j.bbamcr.2012.03.010
  contributor:
    fullname: Hindt
– volume: 37
  start-page: 742
  year: 2001
  ident: B9
  article-title: Increased sulfur amino acids in soybean plants overexpressing the maize 15 kda zein protein.
  publication-title: In Vitro Cell. Dev. Biol. Plant
  doi: 10.1007/s11627-001-0123-x
  contributor:
    fullname: Dinkins
– volume: 98
  start-page: 1128
  year: 1992
  ident: B5
  article-title: Phosphorus nutrition influence on leaf senescence in soybean.
  publication-title: Plant Physiol.
  doi: 10.1104/pp.98.3.1128
  contributor:
    fullname: Crafts-Brandner
– volume: 11
  issue: 152
  year: 2011
  ident: B10
  article-title: Genetic variation of γ -tocopherol methyltransferase gene contributes to elevated α -tocopherol content in soybean seeds.
  publication-title: BMC Plant Biol.
  doi: 10.1186/1471-2229-11-152
  contributor:
    fullname: Dwiyanti
– volume: 224
  start-page: 1116
  year: 2006
  ident: B53
  article-title: Molecular and phenotypic characterization of transgenic soybean expressing the Arabidopsis ferric chelate reductase gene, FRO2.
  publication-title: Planta
  doi: 10.1007/s00425-006-0293-1
  contributor:
    fullname: Vasconcelos
– volume: 93
  start-page: 723
  year: 1990
  ident: B57
  article-title: Physiological characteristics of Fe accumulation in the ‘bronze’ mutant of Pisum sativum L., cv ‘sparkle’ E107 (brz brz).
  publication-title: Plant Physiol.
  doi: 10.1104/pp.93.2.723
  contributor:
    fullname: Welch
– volume: 40
  start-page: 37
  year: 1999
  ident: B26
  article-title: The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range.
  publication-title: Plant Mol. Biol.
  doi: 10.1023/A:1026438615520
  contributor:
    fullname: Korshunova
– volume: 146
  start-page: 268
  year: 1995
  ident: B60
  article-title: Retranslocation of iron from primary leaves of bean plants grown under iron deficiency.
  publication-title: J. Plant Physiol.
  doi: 10.1016/S0176-1617(11)82052-3
  contributor:
    fullname: Zhang
– volume: 42
  start-page: 94
  year: 2001
  ident: B28
  article-title: Technical advance: reduction of Fe(III)-chelates by mesophyll leaf discs of sugar beet. Multi-component origin and effects of Fe deficiency.
  publication-title: Plant Cell Physiol.
  doi: 10.1093/pcp/pce012
  contributor:
    fullname: Larbi
– volume: 48
  start-page: 11640
  year: 2009
  ident: B62
  article-title: Metal binding affinities of Arabidopsis zinc and copper transporters: selectivities match the relative, but not the absolute, affinities of their amino-terminal domains.
  publication-title: Biochemistry
  doi: 10.1021/bi901573b
  contributor:
    fullname: Zimmermann
– start-page: 229
  year: 1991
  ident: B24
  article-title: “Mechanisms of micronutrient uptake and translocation in plants,” in
  publication-title: Micronutrients in Agriculture
  contributor:
    fullname: Kochian
– volume: 177
  start-page: 389
  year: 2008
  ident: B56
  article-title: Whole-plant mineral partitioning throughout the life cycle in Arabidopsis thaliana ecotypes Columbia, Landsberg erecta, Cape Verde Islands, and the mutant line ysl1ysl3.
  publication-title: New Phytol.
  doi: 10.1111/j.1469-8137.2007.02288.x
  contributor:
    fullname: Waters
– volume: 12
  start-page: 101
  year: 2005
  ident: B61
  article-title: Correlation of plant morphological and grain quality traits with mineral element contents in Yunnan rice.
  publication-title: Rice Sci.
  contributor:
    fullname: Zeng
– volume: 10
  start-page: 835
  year: 1996
  ident: B59
  article-title: Genetic evidence that induction of root Fe3+ chelate reductase activity is necessary for iron uptake under iron deficiency.
  publication-title: Plant J.
  doi: 10.1046/j.1365-313X.1996.10050835.x
  contributor:
    fullname: Yi
– volume: 105
  start-page: 407
  year: 1982
  ident: B37
  article-title: Rapid method for measuring changes in pH and reducing processes along roots of intact plants.
  publication-title: Z. Pflanzenphysiol.
  doi: 10.1016/S0044-328X(82)80038-X
  contributor:
    fullname: Marschner
– volume: 185
  start-page: 189
  year: 1989
  ident: B48
  article-title: Physiological disorders of the nicotianamine-auxotroph tomato mutant chloronerva at different levels of iron nutrition. II. Iron deficiency response and heavy metal metabolism.
  publication-title: Biochem. Physiol. Pflanzen
  doi: 10.1016/S0015-3796(89)80080-0
  contributor:
    fullname: Stephan
– volume: 13
  start-page: 231
  year: 1990
  ident: B29
  article-title: Mineral contents of soybean seed coats and embryos during development.
  publication-title: J. Plant Nutr.
  doi: 10.1080/01904169009364070
  contributor:
    fullname: Lazlo
– volume: 54
  start-page: 183
  year: 2003
  ident: B6
  article-title: Iron transport and signaling in plants.
  publication-title: Annu. Rev. Plant Biol.
  doi: 10.1146/annurev.arplant.54.031902.135018
  contributor:
    fullname: Curie
– volume: 122
  start-page: 337
  year: 2000
  ident: B14
  article-title: Iron deficiency decreases the Fe(III)-chelate reducing activity of leaf protoplasts.
  publication-title: Plant Physiol.
  doi: 10.1104/pp.122.2.337
  contributor:
    fullname: Gonzalez-Vallejo
– volume: 276
  start-page: 48775
  year: 2001
  ident: B52
  article-title: Iron prevents ferritin turnover in hepatic cells.
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M105392200
  contributor:
    fullname: Truty
– volume: 190
  start-page: 151
  year: 1993
  ident: B2
  article-title: Iron uptake by leaf mesophyll cells: the role of the plasma membrane-bound ferric-chelate reductase.
  publication-title: Planta
  doi: 10.1007/BF00196606
  contributor:
    fullname: Brüggemann
– volume: 104
  start-page: 649
  year: 1994
  ident: B15
  article-title: Iron transport to developing ovules of Pisum sativum. I. Seed import characteristics and phloem iron-loading capacity of source regions.
  publication-title: Plant Physiol.
  doi: 10.1104/pp.104.2.649
  contributor:
    fullname: Grusak
– volume: 54
  start-page: 583
  year: 2004
  ident: B30
  article-title: Identification and characterization of several new members of the ZIP family of metal transporters in Medicago truncatula.
  publication-title: Plant Mol. Biol.
  doi: 10.1023/B:PLAN.0000038271.96019.aa
  contributor:
    fullname: López-Millán
– volume: 216
  start-page: 541
  year: 2003
  ident: B17
  article-title: Iron uptake, trafficking and homeostasis in plants.
  publication-title: Planta
  doi: 10.1007/s00425-002-0920-4
  contributor:
    fullname: Hell
– volume: 51
  start-page: 91
  year: 2010
  ident: B41
  article-title: 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 long-distance transport.
  publication-title: Plant Cell Physiol.
  doi: 10.1093/pcp/pcp170
  contributor:
    fullname: Rellán-álvarez
– volume: 93
  start-page: 5624
  year: 1996
  ident: B11
  article-title: A novel iron-regulated metal transporter from plants identified by functional expression in yeast.
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.93.11.5624
  contributor:
    fullname: Eide
– volume: 133
  start-page: 1102
  year: 2003
  ident: B3
  article-title: Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control.
  publication-title: Plant Physiol.
  doi: 10.1104/pp.103.025122
  contributor:
    fullname: Connolly
– volume: 182
  start-page: 49
  year: 2009
  ident: B58
  article-title: Biofortification of crops with seven mineral elements often lacking in human diets – iron, zinc, copper, calcium, magnesium, selenium and iodine.
  publication-title: New Phytol.
  doi: 10.1111/j.1469-8137.2008.02738.x
  contributor:
    fullname: White
– volume: 62
  start-page: 379
  year: 2010
  ident: B20
  article-title: Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese.
  publication-title: Plant J.
  doi: 10.1111/j.1365-313X.2010.04158.x
  contributor:
    fullname: Ishimaru
– volume: 8
  start-page: 367
  year: 1998
  ident: B35
  article-title: Iron transport and storage within the seed coat and embryo of developing seeds of pea (Pisum sativum L.)
  publication-title: Seed Sci. Res.
  doi: 10.1017/S0960258500004293
  contributor:
    fullname: Marentes
– volume: 80
  start-page: 175
  year: 1986
  ident: B45
  article-title: Evidence for a specific uptake system for iron phytosiderophores in roots of grasses.
  publication-title: Plant Physiol.
  doi: 10.1104/pp.80.1.175
  contributor:
    fullname: Römheld
– volume: 41
  start-page: 510
  year: 1966
  ident: B50
  article-title: Iron translocation. I. Plant culture, exudate sampling, iron-citrate analysis.
  publication-title: Plant Physiol.
  doi: 10.1104/pp.41.3.510
  contributor:
    fullname: Tiffin
– volume: 14
  start-page: 1223
  year: 2002
  ident: B54
  article-title: IRT1, an Arabidopsis transporter essential for iron uptake from the soil and plant growth.
  publication-title: Plant Cell
  doi: 10.1105/tpc.001388
  contributor:
    fullname: Vert
– year: 1995
  ident: B36
  article-title: Mineral Nutrition of Higher Plants, 2nd Edn.
  contributor:
    fullname: Marschner
– volume: 33
  start-page: 133
  year: 1987
  ident: B40
  article-title: Manganese absorption and transport in rice.
  publication-title: Physiol. Plant.
  doi: 10.1111/j.1399-3054.1975.tb03780.x
  contributor:
    fullname: Ramani
– volume: 63
  start-page: 131
  year: 2012
  ident: B23
  article-title: Iron uptake, translocation, and regulation in higher plants.
  publication-title: Annu. Rev. Plant Biol.
  doi: 10.1146/annurev-arplant-042811-105522
  contributor:
    fullname: Kobayashi
– volume: 5
  start-page: 27
  year: 2012
  ident: B21
  article-title: Fitting into the harsh reality: regulation of iron-deficiency responses in dicotyledonous plants.
  publication-title: Mol. Plant
  doi: 10.1093/mp/ssr065
  contributor:
    fullname: Ivanov
– volume: 201
  start-page: 155
  year: 2013
  ident: B13
  article-title: New Phytol.
  doi: 10.1111/nph.12471
  contributor:
    fullname: Fourcroy
– volume: 223
  start-page: 1178
  year: 2006
  ident: B39
  article-title: Expression profiling of the Arabidopsis ferric chelate reductase (FRO) gene family reveals differential regulation by iron and copper.
  publication-title: Planta
  doi: 10.1007/s00425-005-0165-0
  contributor:
    fullname: Mukherjee
– volume: 397
  start-page: 694
  year: 1999
  ident: B43
  article-title: A ferric-chelate reductase for iron uptake from soils.
  publication-title: Nature
  doi: 10.1038/17800
  contributor:
    fullname: Robinson
– volume: 48
  start-page: 273
  year: 1971
  ident: B51
  article-title: Translocation of nickel in xylem exudates of plants.
  publication-title: Plant Physiol.
  doi: 10.1104/pp.48.3.273
  contributor:
    fullname: Tiffin
– volume: 47
  start-page: 669
  year: 1996
  ident: B8
  article-title: Ferric chelate reduction by sunflower (Helianthus annuus L.) leaves: influence of light, oxygen, iron-deficiency and leaf age.
  publication-title: J. Exp. Bot.
  doi: 10.1093/jxb/47.5.669
  contributor:
    fullname: de la Guardia
– volume: 140
  start-page: 1345
  year: 2006
  ident: B12
  article-title: Light-regulated, tissue-specific, and cell differentiation-specific expression of the Arabidopsis Fe(III)-chelate reductase gene AtFRO6.
  publication-title: Plant Physiol.
  doi: 10.1104/pp.105.074138
  contributor:
    fullname: Feng
– volume: 241
  start-page: 75
  year: 2002
  ident: B1
  article-title: Organic acids and Fe deficiency: a review.
  publication-title: Plant Soil
  doi: 10.1023/A:1016093317898
  contributor:
    fullname: Abadía
– volume: 105
  start-page: 10619
  year: 2008
  ident: B22
  article-title: Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions.
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.0708367105
  contributor:
    fullname: Jeong
– volume: 39
  start-page: 415
  year: 2004
  ident: B25
  article-title: OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem.
  publication-title: Plant J.
  doi: 10.1111/j.1365-313X.2004.02146.x
  contributor:
    fullname: Koike
– volume: 2
  issue: 543
  year: 2012
  ident: B38
  article-title: Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition.
  publication-title: Sci. Rep.
  doi: 10.1038/srep00543
  contributor:
    fullname: Masuda
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Snippet Iron is an important micronutrient in human and plant nutrition. Adequate iron nutrition during crop production is central for assuring appropriate iron...
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SubjectTerms AtFRO2
Iron
Mineral nutrition
Plant Science
Soybean
transgenic
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Title Evaluation of constitutive iron reductase (AtFRO2) expression on mineral accumulation and distribution in soybean (Glycine max. L)
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