Loading and bioavailability of iron in cereal grains

Plant Cell, Tissue and Organ Culture

Volumn 113, Issue 3, 2013, Pages 363-373

  Paul, Soumitra ^a   Ali, Nusrat ^a   Sarkar, Sailendra N ^a   Datta, Swapan K ^a,b   Datta, Karabi ^a  

^a UNIVERSITY OF CALCUTTA   (India)

^b INDIAN COUNCIL OF AGRICULTURAL RESEARCH   (India)

Author keywords

Biotechnology; Cereals; Ferritin; Iron; Phytosiderophores; Transporters

Indexed keywords

ALEURONE LAYERS; CEREAL GRAINS; CEREALS; FERRITIN; PHYTOSIDEROPHORES; PROTEIN FAMILY; ROOT ABSORPTION; TRANSPORTERS;

BIOCHEMISTRY; BIOTECHNOLOGY; CHELATION; IRON; IRON COMPOUNDS; PROTEINS;

LOADING;

EID: 84878187290     PISSN: 01676857     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11240-012-0286-7     Document Type: Review

References (97)

1. Ali N, Datta K, Datta SK (2010) RNA interference in designing transgenic crops. GM Crops 1: 207-213.
2. Aoyama T, Kobyashi T, Takahashi M, Nagasaka S, Usuda K et al (2009) Osysl18 is a rice iron (III)-deoxymugienic acid transporter specifically expressed in reproductive organs and phloem of lamina joints. Plant Mol Biol 70: 681-692.
3. 1) transporter controls iron uptake in plants. Proc Natl Acad Sci USA 108: 12985-12986.
4. Bashir K, Ishimaru Y, Nishizawa NK (2010) Iron uptake and loading into rice grains. Rice 3: 122-130.
5. Bhuiyan MSU, Min SR, Jeong JW, Sultana S, Choi KS, Lee Y, Liu JR (2011a) Overexpression of AtATM3 in Brassicajuncea confers enhanced heavy metal tolerance and accumulation. Plant Cell Tiss Organ Cult 107: 69-77.
6. Bhuiyan MSU, Min SR, Jeong JW, Sultana S, Choi KS, Song YW, Lee Y, Lim YP, Liu JR (2011b) Overexpression of a yeast cadmium factor I (YCF1) enhances heavy metal tolerance and accumulation in Brassicajuncea. Plant Cell Tiss Organ Cult 105: 85-91.
7. Bovell-Benjamin AC, Allen LH, Frankel EN, Guinard JX (1999) Sensor quality and lipid oxidation of maize porridge as affected by iron amino acid chelates and EDTA. J Food Sci 64: 371-376.
8. Briat JF, Ravet K, Arnaud N, Duc C, Boucherez J, Touraiine B, Cellier F, Gaymard F (2010) New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants. Ann Bot 105: 811-822.
9. Brinch-Pedersen H, Borg S, Tauris B, Holm PB (2007) Molecular genetic approaches to increasing mineral availability and vitamin content of cereals. J Cereal Sci 46: 308-326.
10. Cakmak I, Pfeiffer WH, McClafferty B (2010) Biofortification of durum wheat with zinc and iron. Cereal Chem 87: 10-20.
11. Cheng L, Wang F, Shou H, Huang F, Zheng L et al (2007) Mutation in nicotianamine aminotransferase stimulated the Fe(II) acquisition system and led to iron accumulation in rice. Plant Physiol 145: 1647-1657.
12. Conte S, Walker EL (2011) Transporter contributing to iron trafficking in plants. Mol Plant. doi: 10. 1093/mp/ssr015.
13. Coulibaly A, Kouakou B, Chen J (2011) Phytic acid in cereal grains: structure, healthy or harmful ways to reduce phytic acid in cereal grains and their effects on nutritional quality. Am J Plant Nutr Fertil Tech 1: 1-22.
14. Curie C, Cassin G, Couch D, Divol F, Higuchi K et al (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103: 1-11.
15. Datta SK, Khush GS (2002) Improving rice to meet food and nutrient needs: biotechnological approaches. J Crop Prod 6: 229-247.
16. Drakakai G, Christou P, Stoger S (2000) Constitutive expression of soybean ferritin cDNA in transgenic wheat and rice results in increased iron levels in vegetative tissues not in seeds. Transgenic Res 9: 445-452.
17. Drakakai G, Marcel S, Glahn RP, Lund EK, Pariagh S, Fischer R, Christou P, Stoger E (2005) Endosperm specific coexpression of recombinant soybean ferritin and Aspergillus phytase in maize results in significant increases in the levels of bioavailable iron. Plant Mol Biol 59: 869-880.
18. FAO/WHO (1999) Joint FAO/WHO expert committee on food additives. 53rd meeting. WHO, Geneva, Switzerland.
19. Gillespie S and Haddad L (2001) Malnutrition in Asia and the Pacific: nutrition and development series, attacking the double burden of malnutrition in Asia and Pacific. Asian Development Bank, International Food Policy Research Institute, pp 5-14.
20. Glahn RP, Chen SQ, Welch RM, Gregorio GB (2002) Comparison of iron bioavailability from 15 rice genotypes: studies using an invitro digestion/caco 2 cell culture model. J Agr Food Chem 50: 3586-3591.
21. Gomez-Galera S, Sudhakar D, Pelacho AM, Capell T, Christou P (2012) Constitutive expression of a barley Fe phytosiderophore transporter increases alkaline soil tolerance and results in iron partitioning between vegetative and storage tissues under stress. Plant Physiol Biochem 53: 46-53.
22. Gordon N (2003) Iron deficiency and the intellect. Brain Dev 25: 3-8.
23. Goto F, Yoshihara T, Shigemoto N, Toki S, Takaiwa F (1999) Iron fortification of rice seed by the soybean ferritin gene. Nat Biotechnol 17: 282-286.
24. Guerinot ML (2001) Improving rice yields-ironing out the details. Nat Biotechnol 19: 417-418.
25. Haydon MJ, Kawachi M, Wirtz M, Hillmer S, Hell R, Kramer U (2012) Vacuolar Nicotianamine has critical and distinct roles under iron deficiency and for zinc sequestration in Arabidopsis. Plant Cell. doi: 10. 1105/tpc. 111. 095042.
26. Hindt MN, Guerinot ML (2012) Getting a sense for signals: regulation of the plant iron deficiency response. Biochim Biophys Acta. doi: 10. 1016/j. bbamcr. 2012. 03. 010.
27. Hurell RF (2002) Fortification: overcoming technical and practical barriers, forging effective strategies to combat iron deficiency. J Nutr 132: 806-812.
28. Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y et al (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. J Biol Chem 284: 3470-3479.
29. Ishimaru Y, Kim SA, Tsukamoto T, Oki HTK, Watanabe S et al (2007) Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil. Proc Natl Acad Sci USA 104: 7373-7378.
30. Ishimaru Y, Masuda H, Bashir K, Inoue H, Tsukamoto T et al (2010) Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J 62: 379-390.
31. Ishimaru Y, Kakei Y, Shimo H, Bashir K, Sato Y et al (2011) A rice phenolics efflux transporter is essential for solubilizing precipitated apoplasmic iron in the plant stele. J Biol Chem 286: 24649-24655.
32. Johnson AAT, Kyriacou B, Damien L, Callahan DL, Carruthers L, Stangoulis J, Lombi E, Tester M (2011) Constitutive overexpression of the Osnas gene family reveals single-gene strategies for effective iron- and zinc-biofortification of rice endosperm. PLoS ONE 6: e24476.
33. Kakei Y, Yamaguchi I, Kobyashi T, Takahashi M, Nakanishi H, Yamakawa T, Nishizawa NK (2009) A highly sensitive, quick and simple quantification method for nicotianamine and 2'-deoxymugienic acid from minimum samples using LC/ESI-TOF-MS achieves functional analysis of these components in plants. Plant Cell Physiol 50: 1988-1993.
34. Kawai S, Kamei S, Matsuda Y, Ando R, Kondo S, Ishizawa A, Alam S (2001) Concentrations of iron and phytosiderophores in xylem sap of iron-deficient barley plants. Soil Sci Plant Nutr 47: 265-272.
35. Kim SA, Guerinot ML (2007) Mining iron: iron uptake and transport in plants. FEBS Lett 581: 273-2280.
36. King JC (2002) Evaluation the impact of plant biofortification on human biofortication, symposium: plant Breeding: a new tool for fighting micronutrient malnutrition. J Nutr 132: 511-513.
37. Kruger C, Berkowitz O, StephanUdo W, Hell R (2002) A metal-binding member of the late embryogenesis abundant protein family transports iron in the phloem of Ricinus communis L. J Biol Chem 277: 25062-25069.
38. Kuwano M, Mimura T, Takaiwa F, Yoshida KT (2009) Generation of stable 'low phytic acid' transgenic rice through antisense repression of the 1D-myo-inositol 3-phosphate synthase gene (RINO1) using the 18-kDa oleosin promoter. Plant Biotech J 7: 96-105.
39. Lee S, An G (2009) Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant Cell Environ 32: 408-416.
40. Lee S, Chiecko JC, Kim SA, Walker EL, Lee Y, Guerinot ML, An G (2009a) Disruption of Osysl15 leads to iron inefficiency in rice plants. Plant Physiol 150: 786-800.
41. Lee S, Jeon US, Lee SJ, Kim YK, Persson DP et al (2009b) Iron fortification of rice seeds through activation the nicotinamine synthase gene. Proc Natl Acad Sci USA 106: 22014-22019.
42. Lee S, Kim SA, Lee J, Guerinot ML, An G (2010) Zinc deficiency-inducible OsZIP8 encodes a plasma membrane localized zinc transporter in rice. Mol Cells 29: 551-558.
43. Lee S, Persson DP, Hansen TH, Husted S, Schjoerring JK et al (2011) Bio-available zinc in rice seed is increased by activation tagging of nicotianamine synthase. Plant Biotech J 9: 865-873.
44. Lin YF, Liang HM, Yang SY, Boch A, Clemens S et al (2009) Arabidopsis IRT3 is a zinc regulated and plasma membrane localized zinc/iron transporter. New Phytol 182: 392-404.
45. Lombi E, Smith E, Hansen TH, Paterson D, DeJonge MD et al (2011) Megapixel imaging of (micro) nutrients in mature barley grains. J Exp Bot 62: 273-282.
46. Lozoff B, Georgieff MK (2006) Iron deficiency and brain development. Semin Pediatr Neurol 13: 158-165.
47. Lucca P, Hurell R, Potrykus I (2001) Genetic engineering approaches to improve the bioavailability and the level of iron in rice grains. Theor Appl Genet 102: 392-397.
48. Marschner H, Romheld V, Kissel M (1986) Different strategies in higer plants in mobilization and uptake of iron. J Plant Nutr 9: 695-713.
49. Masuda H, Usuda K, Kobyashi T, Ishimaru Y, Kakei Y et al (2009) Overexpression of the barley nicotianamine synthase gene HvNAS1 increases iron and zinc concentrations in rice grains. Rice 2: 155-166.
50. Masuda T, Goto F, Yoshihara T, Mikami B (2010) Crystal structure of plant ferritin reveals a novel metal binding sites that functions as a transit site for the metal transfer in ferritin. J Biol Chem 285: 4049-4059.
51. Moore KL, Zhao FJ, Gritsch CS, Tosi P, Hawkesford MJ, McGrath SP, Shewry PR, Grovenor CRM (2012) Localisation of iron in wheat grain using high resolution secondary ion mass spectroscopy. J Cereal Sci 55: 183-187.
52. Morrissey J, Guerinot ML (2009) Iron uptake and transport in plants: the good, the bad and the ionome. Chem Rev 109: 4553-4567.
53. Negishi T, Nakanishi H, Yazaki J, Kishimoto N, Fujii F et al (2002) cDNA microarray analysis of gene expression during Fe-deficiency stress in barley suggests that polar transport of vesicles is implicated in phytosiderophore secretion in Fe-deficient barley roots. Plant J 30: 83-94.
54. Nozoye T, Inoue H, Takahashi M, Ishimaru Y, Nakanishi H, Mori S, Nishizawa NK (2007) The expression of iron homeostasis-related genes during rice germination. Plant Mol Biol 64: 35-47.
55. Nozoye T, Nagasaka S, Kobyashi T, Takahashi M, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 286: 5446-5454.
56. Ogo Y, Itai RN, Nakanishi H, Kobayashi T, Takahashi M, Mori S, Nishizawa NK (2007) The rice bHLH protein OslRO2 is an essential regulator of the genes involved in Fe uptake under Fe-deficient conditions. Plant J 51: 366-377.
57. Ozturk L, Yazici MA, Yucel C, Torum A, Cekic C, Bagci A, Ozkan H, Barun HJ, Sayers Z, Cakmak I (2006) Concentration and localization of zinc during seed development and germination in wheat. Physiol Plantarum 128: 144-152.
58. Paul S, Ali N, Gayen D, Datta SK, Datta K (2012) Molecular breeding of Osfer2 gene to increase iron nutrition in rice. GM Crop Food 3: 310-316.
59. Persson DP, Hansen TH, Laursen KH, Schjoerring JK, Husted S (2009) Simultaneousiron, zinc, sulfur and phosphorus speciation analysis of barley grain tissues using SEC-ICP-MS and IP-ICP-MS. Metallomics 1: 418-426.
60. Qu LQ, Takaiwa F (2004) Evaluation of tissue specificity and expression strength of rice seed component gene promoters in transgenic rice. Plant Biotech J 2: 113-125.
61. Qu L, Yoshihara T, Ooyama A, Goto F, Takaiwa F (2005) Iron accumulation does not parallel the high expression of ferritin in transgenic rice seeds. Planta 222: 225-233.
62. Raboy V (2007) The ABCs of low-phytate crops. Nat Biotechnol 25: 874-875.
63. Ramirez M, Simontacchi M, Murgia I, Zabaleta E, Lamattina L (2011) Nitric oxide, nitrosyl iron complexes, ferritin and frataxin: a well equipped team to preserve plant iron homeostasis. Plant Sci 181: 582-592.
64. Ravet K, Touraine B, Boucherez J, Briat JF, Gaymard F, Cellier F (2009) Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J 57: 400-412.
65. Regvar M, Eichert D, Kaulich B, Gianoncelli A, Pongrac P, Vogel-Mikus K, Kreft I (2011) New insights into globoids of protein storage vacuoles in wheat aleurone using synchrotron soft X-ray microscopy. J Exp Bot 62: 3929-3939.
66. Ricachenevsky FK, Sperotto RA, Menguer PK, Sperb ER, Lopes KL, Fett JP (2011) ZINC-INDUCED FACILITATOR-l LIKE family in plants: lineage specific expansion in monocotyledons and conserved genomic and expression features among rice (Oryza sativa) paralogs. BMC Plant Biol 11: 1-22.
67. Shi J, Wang H, Schellin K, Li B, Faller M et al (2007) Embryo-specific silencing of a transporter reduces phytic acid content of maize and soybean seeds. Nat Biotechnol 25: 930-937.
68. Smart KE, Smith JAC, Kilburn MR, Martin BGH, Hawes C, Grovenor CRM (2010) High-resolution elemental localization in vacuolate plant cells by nanoscale secondary ion mass spectrometry. Plant J 63: 870-879.
69. Song SY, Chen Y, Chen J, Dai XY, Zhang WH (2011) Physiological mechanisms underlying OsNAC5-dependent tolerance of rice plants to abiotic stress. Planta 234: 331-345.
70. Sperotto RA, Ricachenevsky FK, Duarte GL, Boff KL, Lopes KL, Sperb ER, Fett JP (2009) Identification of up-regulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABA-dependent transcription factor. Planta 230: 985-1002.
71. Stein AJ, Meenakshi JV, Qaim M, Nestel P, Sachdev HPS, Bhutta AZ (2008) Potential impacts of iron biofortification in India. Soc Sci Med 66: 1797-1808.
72. Stein RJ, Ricachenevsky FK, Fett JP (2009) Differential regulation of two rice ferritin genes (OsFER1 and OsFER2). Plant Sci 177: 563-569.
73. Stevenson-Paulik J, Bastidas RJ, Chiou ST, Frye RA, York JD (2005) Generation of phytate-free seeds in Arabidopsis through disruption of inositol polyphosphate kinases. Proc Natl Acad Sci USA 102: 12612-12617.
74. Suzuki M, Tanaka K, Kuwano M, Yoshida KT (2007) Expression pattern of inositol phosphate-related enzymes in rice (Oryza sativa L): implications for the phytic acid biosynthetic pathway. Gene 405: 55-64.
75. Suzuki M, Morikawa KC, Nakanishi H, Takahashi M, Saigusa M, Mori S, Nishizawa NK (2008) Transgenic rice lines that include barley genes have increased tolerance to low iron availability in a calcareous paddy soil. Soil Sci Plant Nutr 54: 77-85.
76. Takahashi M, Nakanishi H, Kawasaki S, Nishizawa NK, Mori S (2001) Enhanced tolerance to rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. Nat Biotechnol 19: 466-469.
77. Takahashi M, Terada Y, Nakai I, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2003) Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. Plant Cell 15: 1263-1280.
78. Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genom 284: 173-183.
79. Tauris B, Borg S, Gregersen PL, Holm PB (2009) A roadmap for zinc trafficking in the developing barley grain based on laser capture microdissection and gene expression profiling. J Exp Bot 60: 1333-1347.
80. Theil EC (2003) Ferritin: at the crossroads of iron and oxygen metabolism. In: Metal-binding proteins and trace element metabolism. J Nutr 133: 1549-1553.
81. Vasconcelos M, Datta K, Oliva N, Khalekuzzaman M, Torrizo L, Krishnan S, Oliveira M, Goto F, Datta SK (2003) Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. Plant Sci 164: 371-378.
82. Vasconcelos M, Musetti V, Li C, Datta SK, Grusak MA (2004) Functional analysis of transgenic rice (Oryza sativa L.) transformed with Arabidopsis thaliana ferric reductase (Atfro2). Soil Sci Plant Nutr 50: 1151-1157.
83. Vert G, Briat JF, Curie C (2001) Arabidopsis IRT2 gene encodes a root-periphery iron transporter. Plant J 26: 181-189.
84. 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 plant growth. Plant Cell 14: 1223-1233.
85. von Wiren N, Klair S, Bansal S, Briat J, Khodr H, Shioiri RA, Leigh R, Hider C (1999) Nicotianamine chelates both Fe III and Fe II. Implications for metal transport in plants. Plant Physiol 119: 1107-1114.
86. Walker EL, Waters BM (2011) The role of transition metal homeostasis in plant seed development. Curr Opin Plant Biol 14: 318-324.
87. Wang YX, Specht A, Horst WJ (2011) Stable isotope labeling and zinc distribution in grains studied by laser ablation ICP-MS in an ear culture system reveals zinc transport barriers during grain filling in wheat. New Phytol 189: 428-437.
88. Waters BM, Sankaran RP (2011) Moving micronutrients from soil to seeds: genes and physiological process from a biofortification perspective. Plant Sci 180: 562-574.
89. WHO (2002) The World Health Report. Geneva, WHO publishing web. http://www. who. int/nutrition/topics/ida.
90. WHO (2008) Micronutrient deficiencies: iron deficiency anemia. Geneva, WHO publishing web. http://www. who. int/nutrition/topics/ida.
91. Writh J, Poletti S, Aeschlimann B, Yakandawala N, Drosse B et al (2009) Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin. Plant Biotech J 7: 631-644.
92. Yamaji N, Ma JF (2009) A transporter at the node responsible for intervascular transfer of silicon in rice. Plant Cell 21: 2878-2883.
93. Yokosho K, Yamaji N, Ueno D, Mitani N, Ma JF (2009) OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol 149: 297-305.
94. Zancani M, Peresson C, Biroccio A, Federici G, Urbani A et al (2004) Evidence for the presence of ferritin in plant mitochondria. Eur J Biochem 271: 3657-3664.
95. Zheng L, Cheng Z, Ai C, Jiang X, Bei X et al (2010) Nicotianamine, a novel enhancer of rice iron bioavailability to humans. PLoS ONE 5: e10190.
96. Zheng L, Fuji M, Yamaji N, Sasaki A, Yamane M, Sakurai I, Sato K, Ma JF (2011) Isolation and charecterisation of barley yellow stripe-like gene Hvysl5. Plant Cell Physiol 52: 765-774.
97. Zok A, Olah R, Hideg E, Horvath VG, Kos PB, Majer P, Varadi GY, Szegedi E (2010) Effect of Medicago sativa ferritin gene on stress tolerance in transgenic grapevine. Plant Cell Tiss Organ Cult 100: 339-344.