Iron homeostasis in plants-a brief overview

Metallomics

Volumn 9, Issue 7, 2017, Pages 813-823

  Connorton, James M ^a   Balk, Janneke ^a   Rodríguez Celma, Jorge ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRON TRANSPORT PROPERTIES; HISTOLOGY; PLANTS (BOTANY); STRUCTURAL GEOLOGY; TISSUE; TRANSCRIPTION;

BIOFORTIFICATION; BIOTECHNOLOGICAL APPROACHES; ELECTRON TRANSPORT CHAIN; ENZYME COFACTORS; IRON CONCENTRATIONS; IRON HOMEOSTASIS; POST-TRANSCRIPTIONAL; REGULATORY MECHANISM;

IRON COMPOUNDS;

IRON;

BIOFORTIFICATION; BIOSYNTHESIS; HOMEOSTASIS; IRON STORAGE; IRON TRANSPORT; PRIORITY JOURNAL; REGULATORY MECHANISM; RESPIRATORY CHAIN; REVIEW; CROP; METABOLISM; PLANT; TRANSPORT AT THE CELLULAR LEVEL;

BIOFORTIFICATION; BIOLOGICAL TRANSPORT; CROPS, AGRICULTURAL; HOMEOSTASIS; IRON; PLANTS;

EID: 85025108776     PISSN: 17565901     EISSN: 1756591X     Source Type: Journal    
DOI: 10.1039/c7mt00136c     Document Type: Review

References (126)

1. T. Kobayashi N. K. Nishizawa Iron uptake, translocation, and regulation in higher plants Annu. Rev. Plant Biol. 2012 63 131 152
2. T. Brumbarova P. Bauer R. Ivanov Molecular mechanisms governing Arabidopsis iron uptake Trends Plant Sci. 2015 20 124 133
3. W. Li P. Lan The understanding of the plant iron deficiency responses in Strategy I plants and the role of ethylene in this process by omic approaches Front. Plant Sci. 2017 8 40
4. H. H. Tsai W. Schmidt Mobilization of iron by plant-borne coumarins Trends Plant Sci. 2017 22 538 548
5. J. Balk T. A. Schaedler Iron cofactor assembly in plants Annu. Rev. Plant Biol. 2014 65 125 153
6. M. W. Vasconcelos W. Gruissem N. K. Bhullar Iron biofortification in the 21st century: setting realistic targets, overcoming obstacles, and new strategies for healthy nutrition Curr. Opin. Biotechnol. 2017 44 8 15
7. V. Römheld H. Marschner Evidence for a specific uptake system for iron phytosiderophores in roots of grasses Plant Physiol. 1986 80 175 180
8. N. J. Robinson C. M. Procter E. L. Connolly M. L. Guerinot A ferric-chelate reductase for iron uptake from soils Nature 1999 397 694 697
9. D. Eide M. Broderius J. Fett M. L. Guerinot A novel iron-regulated metal transporter from plants identified by functional expression in yeast Proc. Natl. Acad. Sci. U. S. A. 1996 93 5624 5628
10. S. Santi W. Schmidt Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots New Phytol. 2009 183 1072 1084
11. K. Higuchi et al., Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores Plant Physiol. 1999 119 471 480
12. T. Nozoye et al., Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants J. Biol. Chem. 2011 286 5446 5454
13. C. Curie et al., Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake Nature 2001 409 346 349
14. H. Inoue et al., 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 J. Biol. Chem. 2009 284 3470 3479
15. S. Cesco G. Neumann N. Tomasi R. Pinton L. Weisskopf Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition Plant Soil 2010 329 1 25
16. C. W. Jin et al., Iron deficiency-induced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover Plant Physiol. 2007 144 278 285
17. J. Rodríguez-Celma et al., Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula Plant Physiol. 2013 162 1473 1485
18. P. Fourcroy et al., Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency New Phytol. 2014 201 155 167
19. N. B. Schmid et al., Feruloyl-CoA 6′-Hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis Plant Physiol. 2014 164 160 172
20. K. Kai et al., Scopoletin is biosynthesized via ortho-hydroxylation of feruloyl CoA by a 2-oxoglutarate-dependent dioxygenase in Arabidopsis thaliana Plant J. 2008 55 989 999
21. P. Sisó-Terraza et al., Accumulation and secretion of coumarinolignans and other coumarins in Arabidopsis thaliana roots in response to iron deficiency at high pH Front. Plant Sci. 2016 7 1711
22. C. Zamioudis J. Hanson C. M. J. Pieterse β-Glucosidase BGLU42 is a MYB72-dependent key regulator of rhizobacteria-induced systemic resistance and modulates iron deficiency responses in Arabidopsis roots J. Physiol. 2014 204 368 379
23. P. Sisó-Terraza J. J. Rios J. Abadía A. Abadía A. Álvarez-Fernández Flavins secreted by roots of iron-deficient Beta vulgaris enable mining of ferric oxide via reductive mechanisms New Phytol. 2016 209 733 745
24. X. F. Zhu B. Wang W. F. Song S. J. Zheng R. F. Shen Putrescine alleviates iron deficiency via NO-dependent reutilization of root cell-wall Fe in Arabidopsis Plant Physiol. 2016 170 558 567
25. 2+ transport system Mol. Plant 2016 9 485 488
26. 2 Plant J. 2006 45 335 346
27. P. Pedas et al., Manganese efficiency in barley: identification and characterization of the metal ion transporter HvIRT1 Plant Physiol. 2008 148 455 466
28. D. J. R. Lane et al., Cellular iron uptake, trafficking and metabolism: Key molecules and mechanisms and their roles in disease Biochim. Biophys. Acta, Mol. Cell Res. 2015 1853 1130 1144
29. L. D. Palmer E. P. Skaar Transition metals and virulence in bacteria Annu. Rev. Genet. 2016 50 67 91
30. M. Barberon et al., Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis Proc. Natl. Acad. Sci. U. S. A. 2014 111 8293 8298
31. G. Dubeaux E. Zelazny G. Vert Getting to the root of plant iron uptake and cell-cell transport: polarity matters! Commun. Integr. Biol. 2015 8 e1038441
32. L. Castaings et al., The high-affinity metal transporters NRAMP1 and IRT1 team up to take up iron under sufficient metal provision Sci. Rep. 2016 6 37222
33. M. Barberon The endodermis as a checkpoint for nutrients New Phytol. 2017 213 1604 1610
34. M. Barberon et al., Adaptation of root function by nutrient-induced plasticity of endodermal differentiation Cell 2016 164 447 459
35. H. Inoue et al., 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 Plant J. 2003 36 366 381
36. M. Klatte et al., The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses Plant Physiol. 2009 150 257 271
37. J. Bonneau U. Baumann J. Beasley Y. Li A. A. T. Johnson Identification and molecular characterization of the nicotianamine synthase gene family in bread wheat Plant Biotechnol. J. 2016 14 2228 2239
38. R. J. DiDonato L. A. Roberts T. Sanderson R. B. Eisley E. L. Walker Arabidopsis Yellow Stripe-Like2 (YSL2): A metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes Plant J. 2004 39 403 414
39. J. Morrissey et al., The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis Plant Cell 2009 21 3326 3338
40. R. Rellán-Alvarez et al., 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 Plant Cell Physiol. 2010 51 91 102
41. L. S. Green E. E. Rogers FRD3 controls iron localization in Arabidopsis Plant Physiol. 2004 136 2523 2531
42. K. Yokosho N. Yamaji J. F. Ma OsFRDL1 expressed in nodes is required for distribution of iron to grains in rice J. Exp. Bot. 2016 67 5485 5494
43. G. Finazzi et al., Ions channels/transporters and chloroplast regulation Cell Calcium 2015 58 86 97
44. K. Bashir S. Rasheed T. Kobayashi M. Seki N. K. Nishizawa Regulating subcellular metal homeostasis: the key to crop improvement Front. Plant Sci. 2016 7 1192
45. Z. Zhai et al., OPT3 is a phloem-specific iron transporter that is essential for systemic iron signaling and redistribution of iron and cadmium in Arabidopsis Plant Cell 2014 26 2249 2264
46. D. G. Mendoza-Cózatl et al., OPT3 is a component of the iron-signaling network between leaves and roots and misregulation of OPT3 leads to an over-accumulation of cadmium in seeds Mol. Plant 2014 7 1455 1469
47. M. Le Jean A. Schikora S. Mari J.-F. Briat C. Curie A loss-of-function mutation in AtYSL1 reveals its role in iron and nicotianamine seed loading Plant J. 2005 44 769 782
48. L. Grillet et al., Ascorbate efflux as a new strategy for iron reduction and transport in plants J. Biol. Chem. 2014 289 2515 2525
49. S. A. Kim et al., Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1 Science 2006 314 1295 1298
50. H. Roschzttardtz G. Conéjéro C. Curie S. Mari Identification of the endodermal vacuole as the iron storage compartment in the Arabidopsis embryo Plant Physiol. 2009 151 1329 1338
51. V. Lanquar et al., Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron EMBO J. 2005 24 4041 4051
52. V. Mary et al., Bypassing iron storage in endodermal vacuoles rescues the iron mobilization defect in the nramp3 nramp4 double mutant Plant Physiol. 2015 169 748 759
53. Y. Zhang Y.-H. Xu H.-Y. Yi J.-M. Gong Vacuolar membrane transporters OsVIT1 and OsVIT2 modulate iron translocation between flag leaves and seeds in rice Plant J. 2012 72 400 410
54. W. Zhu et al., Vacuolar iron transporter BnMEB2 is involved in enhancing iron tolerance of Brassica napus Front. Plant Sci. 2016 7 1353
55. E. C. Theil Ferritin protein nanocages use ion channels, catalytic sites, and nucleation channels to manage iron/oxygen chemistry Curr. Opin. Chem. Biol. 2011 15 304 311
56. M. Zielińska-Dawidziak Plant ferritin - A source of iron to prevent its deficiency Nutrients 2015 7 1184 1201
57. B. Kyriacou et al., Localization of iron in rice grain using synchrotron X-ray fluorescence microscopy and high resolution secondary ion mass spectrometry J. Cereal Sci. 2014 59 173 180
58. J. J. R. Fraústo da Silva and R. J. P. Williams, The biological chemistry of the elements: The inorganic chemistry of life, Oxford University Press, 2001
59. N. A. Espinas et al., Allocation of heme is differentially regulated by ferrochelatase isoforms in Arabidopsis cells Front. Plant Sci. 2016 7 1326
60. P. Brzezowski A. S. Richter B. Grimm Regulation and function of tetrapyrrole biosynthesis in plants and algae Biochim. Biophys. Acta 2015 1847 968 985
61. M. Scharfenberg et al., Functional characterization of the two ferrochelatases in Arabidopsis thaliana Plant, Cell Environ. 2015 38 280 298
62. J. Couturier B. Touraine J.-F. Briat F. Gaymard N. Rouhier The iron-sulfur cluster assembly machineries in plants: current knowledge and open questions Front. Plant Sci. 2013 4 259
63. A. Picciocchi R. Douce C. Alban The plant biotin synthase reaction: Identification and characterization of essential mitochondrial accessory protein components J. Biol. Chem. 2003 278 24966 24975
64. Y. Takahashi A. Mitsui Y. Fujita H. Matsubara Roles of ATP and NADPH in formation of the Fe-S cluster of spinach ferredoxin Plant Physiol. 1991 95 104 110
65. D. Van Hoewyk et al., Chloroplast iron-sulfur cluster protein maturation requires the essential cysteine desulfurase CpNifS Proc. Natl. Acad. Sci. U. S. A. 2007 104 5686 5691
66. X. Hu Y. Kato A. Sumida A. Tanaka R. Tanaka The SUFBC 2 D complex is required for the biogenesis of all major classes of plastid Fe-S proteins Plant J. 2017 90 235 248
67. D. J. A. Netz J. Mascarenhas O. Stehling A. J. Pierik R. Lill Maturation of cytosolic and nuclear iron-sulfur proteins Trends Cell Biol. 2013 24 303 312
68. D. G. Bernard Y. Cheng Y. Zhao J. Balk An allelic mutant series of ATM3 reveals its key role in the biogenesis of cytosolic iron-sulfur proteins in Arabidopsis Plant Physiol. 2009 151 590 602
69. T. A. Schaedler et al., A conserved mitochondrial ATP-binding cassette transporter exports glutathione polysulfide for cytosolic metal cofactor assembly J. Biol. Chem. 2014 289 23264 23274
70. D. Buzas M. Nakamura T. Kinoshita Epigenetic role for the conserved Fe-S cluster biogenesis protein AtDRE2 in Arabidopsis thaliana Proc. Natl. Acad. Sci. U. S. A. 2014 111 13565 13570
71. X. Wang et al., The cytosolic Fe-S cluster assembly component MET18 is required for the full enzymatic activity of ROS1 in active DNA demethylation Sci. Rep. 2016 6 26443
72. C. G. Duan et al., MET18 connects the cytosolic iron-sulfur cluster assembly pathway to active DNA demethylation in Arabidopsis PLoS Genet. 2015 11 1 19
73. Y. F. Han et al., The cytosolic iron-sulfur cluster assembly protein MMS19 regulates transcriptional gene silencing, DNA repair, and flowering time in Arabidopsis PLoS One 2015 10 1 21
74. E. L. Bastow K. Bych J. C. Crack N. E. Le Brun J. Balk NBP35 interacts with DRE2 in the maturation of cytosolic iron-sulfur proteins in Arabidopsis thaliana Plant J. 2017 89 590 600
75. G. Li H. J. Kronzucker W. Shi The response of the root apex in plant adaptation to iron heterogeneity in soil Front. Plant Sci. 2016 7 1 7
76. J. Mora-Macías et al., Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate Proc. Natl. Acad. Sci. U. S. A. 2017 114 E3563 E3572
77. H.-Q. Ling P. Bauer Z. Bereczky B. Keller M. Ganal The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots Proc. Natl. Acad. Sci. U. S. A. 2002 99 13938 13943
78. E. P. Colangelo M. L. Guerinot The essential basic Helix-Loop-Helix protein FIT1 is required for the iron deficiency response Plant Cell 2004 16 3400 3412
79. M. Jakoby H. Y. Wang W. Reidt B. Weisshaar P. Bauer FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana FEBS Lett. 2004 577 528 534
80. Y. X. Yuan J. Zhang D. W. Wang H. Q. Ling AtbHLH29 of Arabidopsis thaliana is a functional ortholog of tomato FER involved in controlling iron acquisition in strategy I plants Cell Res. 2005 15 613 621
81. Y. Yuan et al., FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis Cell Res. 2008 18 385 397
82. N. Wang et al., Requirement and functional redundancy of Ib subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana Mol. Plant 2013 6 503 513
83. A. B. Sivitz V. Hermand C. Curie G. Vert Arabidopsis bHLH100 and bHLH101 control iron homeostasis via a FIT-independent pathway PLoS One 2012 7 e44843
84. T. A. Long et al., The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots Plant Cell 2010 22 2219 2236
85. J. Zhang et al., The bHLH transcription factor bHLH104 interacts with IAA-LEUCINE RESISTANT3 and modulates iron homeostasis in Arabidopsis Plant Cell 2015 27 787 805
86. X. Li H. Zhang Q. Ai G. Liang D. Yu Two bHLH transcription factors, bHLH34 and bHLH104, regulate iron homeostasis in Arabidopsis thaliana Plant Physiol. 2016 170 2478 2493
87. C. M. Palmer M. N. Hindt H. Schmidt S. Clemens M. L. Guerinot MYB10 and MYB72 are required for growth under iron-limiting conditions PLoS Genet. 2013 9 e1003953
88. J. Y. Yan et al., A WRKY transcription factor regulates Fe translocation under Fe deficiency Plant Physiol. 2016 171 2017 2027
89. T. Kobayashi et al., Identification of novel cis-acting elements, IDE1 and IDE2, of the barley IDS2 gene promoter conferring iron-deficiency-inducible, root-specific expression in heterogeneous tobacco plants Plant J. 2003 36 780 793
90. T. Kobayashi et al., The transcription factor IDEF1 regulates the response to and tolerance of iron deficiency in plants Proc. Natl. Acad. Sci. U. S. A. 2007 104 19150 19155
91. Y. Ogo et al., The rice bHLH protein OsIRO2 is an essential regulator of the genes involved in Fe uptake under Fe-deficient conditions Plant J. 2007 51 366 377
92. T. Kobayashi et al., The spatial expression and regulation of transcription factors IDEF1 and IDEF2 Ann. Bot. 2010 105 1109 1117
93. L. Zheng et al., Identification of a novel iron regulated basic helix-loop-helix protein involved in Fe homeostasis in Oryza sativa BMC Plant Biol. 2010 10 166
94. L.-J. Shin et al., IRT1 DEGRADATION FACTOR1, a RING E3 ubiquitin ligase, regulates the degradation of IRON-REGULATED TRANSPORTER1 in Arabidopsis Plant Cell 2013 25 3039 3051
95. S. Lingam et al., Interaction between the bHLH transcription factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis Plant Cell 2011 23 1815 1829
96. J. Meiser S. Lingam P. Bauer Posttranslational regulation of the iron deficiency Basic Helix-Loop-Helix transcription factor FIT is affected by iron and nitric oxide Plant Physiol. 2011 157 2154 2166
97. D. Selote R. Samira A. Matthiadis J. W. Gillikin T. A. Long Iron-binding E3 ligase mediates iron response in plants by targeting basic Helix-Loop-Helix transcription factors Plant Physiol. 2015 167 273 286
98. T. Kobayashi et al., Iron-binding haemerythrin RING ubiquitin ligases regulate plant iron responses and accumulation Nat. Commun. 2013 4 2792
99. M. S. Fan et al., Evidence of decreasing mineral density in wheat grain over the last 160 years J. Trace Elem. Med. Biol. 2008 22 315 324
100. C. Uauy A. Distelfeld T. Fahima A. Blechl J. A. Dubcovsky NAC Gene regulating senescence improves grain protein, zinc, and iron content in wheat Science 2006 314 1298 1301
101. H. S. Randhawa et al., Application of molecular markers to wheat breeding in Canada Plant Breed. 2013 132 458 471
102. M. W. Blair P. Izquierdo Use of the advanced backcross-QTL method to transfer seed mineral accumulation nutrition traits from wild to Andean cultivated common beans Theor. Appl. Genet. 2012 125 1015 1031
103. B. S. Kodkany et al., Biofortification of pearl millet with iron and zinc in a randomized controlled trial increases absorption of these minerals above physiologic requirements in young children J. Nutr. 2013 143 1489 1493
104. J. L. Finkelstein et al., A randomized trial of iron-biofortified pearl millet in school children in India J. Nutr. 2015 145 1576 1581
105. J. D. Haas et al., Consuming iron biofortified beans increases iron status in Rwandan women after 128 days in a randomized controlled feeding trial J. Nutr. 2016 146 1586 1592
106. A. A. T. Johnson et al., Constitutive overexpression of the OsNAS gene family reveals single-gene strategies for effective iron- and zinc-biofortification of rice endosperm PLoS One 2011 6 e24476
107. N. Narayanan et al., Overexpression of Arabidopsis VIT1 increases accumulation of iron in cassava roots and stems Plant Sci. 2015 240 170 181
108. S. Borg et al., Wheat ferritins: Improving the iron content of the wheat grain J. Cereal Sci. 2012 56 204 213
109. J. M. Connorton et al., Functional analysis of vacuolar iron transporters in wheat (Triticum aestivum) identifies TaVIT2 as an iron and manganese transporter effective for biofortification of cereals Plant Physiol. 2017
110. I. H. Slamet-Loedin S. E. Johnson-Beebout S. Impa N. Tsakirpaloglou Enriching rice with Zn and Fe while minimizing Cd risk Front. Plant Sci. 2015 6 1 9
111. R. Banakar A. Álvarez Fernández J. Abadía T. Capell P. Christou The expression of heterologous Fe (III) phytosiderophore transporter HvYS1 in rice increases Fe uptake, translocation and seed loading and excludes heavy metals by selective Fe transport Plant Biotechnol. J. 2016 15 423 432
112. K. V. Krasileva et al., Uncovering hidden variation in polyploid wheat Proc. Natl. Acad. Sci. U. S. A. 2017 114 E913 E921
113. R. Hurrell I. Egli Iron bioavailability and dietary reference values Am. J. Clin. Nutr. 2010 91 1461S 1467S
114. V. Raboy K. A. Young J. A. Dorsch A. Cook Genetics and breeding of seed phosphorus and phytic acid J. Plant Physiol. 2001 158 489 497
115. J. Wirth et al., Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin Plant Biotechnol. J. 2009 7 631 644
116. N. Yamaji et al., Reducing phosphorus accumulation in rice grains with an impaired transporter in the node Nature 2017 541 92 95
117. T. Eagling A. A. Wawer P. R. Shewry F. Zhao S. J. Fairweather-tait Iron bioavailability in two commercial cultivars of wheat: comparison between wholegrain and white flour and the effects of nicotianamine and 2′-deoxymugineic acid on iron uptake into Caco-2 cells J. Agric. Food Chem. 2014 62 10320 10325
118. F. Leenhardt M. A. Levrat-Verny E. Chanliaud C. Rémésy Moderate decrease of pH by sourdough fermentation is sufficient to reduce phytate content of whole wheat flour through endogenous phytase activity J. Agric. Food Chem. 2005 53 98 102
119. G. O. Latunde-Dada et al., Micromilling enhances iron bioaccessibility from wholegrain wheat J. Agric. Food Chem. 2014 62 11222 11227
120. Y. Kakei et al., Development of a novel prediction method of cis-elements to hypothesize collaborative functions of cis-element pairs in iron-deficient rice Rice 2013 6 22
121. A. Koryachko et al., Clustering and Differential Alignment Algorithm: Identification of early stage regulators in the Arabidopsis thaliana iron deficiency response PLoS One 2015 10 1 21
122. H.-J. Mai S. Pateyron P. Bauer Iron homeostasis in Arabidopsis thaliana: transcriptomic analyses reveal novel FIT-regulated genes, iron deficiency marker genes and functional gene networks BMC Plant Biol. 2016 16 211
123. T. Kobayashi et al., The rice transcription factor IDEF1 is essential for the early response to iron deficiency, and induces vegetative expression of late embryogenesis abundant genes Plant J. 2009 60 948 961
124. Y. Ogo et al., A novel NAC transcription factor, IDEF2, that recognizes the Iron Deficiency-Responsive Element 2 regulates the genes involved in iron homeostasis in plants J. Biol. Chem. 2008 283 13407 13417
125. K. R. Trijatmiko et al., Biofortified indica rice attains iron and zinc nutrition dietary targets in the field Sci. Rep. 2016 6 19792
126. S. P. Singh B. Keller W. Gruissem N. K. Bhullar Rice NICOTIANAMINE SYNTHASE 2 expression improves dietary iron and zinc levels in wheat Theor. Appl. Genet. 2017 130 283 292