Enriching rice with Zn and Fe while minimizing Cd risk

Frontiers in Plant Science

Volumn 6, Issue MAR, 2015, Pages

  Slamet Loedin, Inez H ^a   Johnson Beebout, Sarah E ^a   Impa, Somayanda ^a   Tsakirpaloglou, Nikolaos ^a  

^a INTERNATIONAL RICE RESEARCH INSTITUTE   (Philippines)

Author keywords

Agronomic biofortification; Cd contamination; Fe enriched rice; Genetic biofortification; Rice; Risk mitigation; Zn enriched rice

Indexed keywords

EID: 84928016183     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00121     Document Type: Article

References (96)

1. Anuradha, K., Agarwal, S., Batchu, A. K., Babu, A. P., Swamy, B. P. M., Longvah, T., et al. (2012). Evaluatingrice germplasm for ironandzinc concentrationin brown rice and seed dimensions. J. Phytol. 4, 19-25.
2. Arao, T., and Ishikawa, S. (2006). Genotypic differences in cadmium concentration and distribution of soybean and rice. Jpn. Agric. Res. Q. 40, 21-30. doi: 10.6090/jarq.40.21
3. Aung, M. S., Masuda, H., Kobayashi, T., Nakanishi, H.,Yamakawa, T., and Nishizawa, N. K. (2013). Iron biofortification of Myanmar rice. Front. Plant Sci. 4:158. doi: 10.3389/fpls.2013.00158
4. Bashir, K., Takahashi, R., Nakanishi, H., and Nishizawa, N. K. (2013a). The road to micronutrient biofortification of rice: progress and prospects. Front. PlantSci. 4:15. doi: 10.3389/fpls.2013.00015
5. Bashir, K., Takahashi, R., Akhtar, S., Ishimaru, Y., Nakanishi, H., and Nishizawa, N. K. (2013b). The knockdown of OsVIT2 and MIT affects iron localization in rice seed. Rice (N. Y.) 6, 31. doi: 10.1186/1939-8433-6-31
6. Black, R. E., Victora, C. G., Walker, S. P., Bhutta, Z. A., Christian, P., de Onis, M., etal. (2013). Maternal and child undernutrition and overweight in low- income and middle-income countries. Lancet 382, 427-451. doi: 10.1016/S0140-6736(13)60937-X
7. Bostick, B. C., Hansel, C. M., La Force, M. J., and Fendorf, S. (2001). Seasonalfluc- tuations in zinc speciation within a contaminated wetland. Environ. Sci. Technol. 35, 3823-3829. doi: 10.1021/es010549d
8. Bouis, H. E., Hotz, C., Mc Clafferty, B., Meenakshi, J. V., and Pfeiffer, W. H. (2011). Biofortification: A new tool to reduce micronutrient malnutrition. Food Nutr. Bull. 32, S31-S40. doi: 10.1021/es010549d
9. Bouman, B., Barker, R., Humphreys, E., Tuong, T. P., Atlin, G., Bennett, J., et al. (2007). Rice: Feeding the billion, in Water for Food, Water for Life: A Comprehensive Assessment of Water Management in Agriculture, Ed. D. Molden (London: Earthscan and Colombo: International Water Management Institute), 515-549.
10. Briat, J. F., Ravet, K., Arnaud, N., Duc, C., Boucherez, J., Touraine, B., et al. New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants. Ann. Bot. 105, 811-822. doi: 10.1093/aob/mcp128
11. Cakmak, I. (2009). Enrichment of fertilizers with zinc: An excellent investment for humanity and crop production in India. J. Trace Elem. Med. Biol. 23, 281-289. doi: 10.1016/j.jtemb.2009.05.002
12. Cakmak, I., Pfeiffer, W. H., and Mc Clafferty, B. (2010). Biofortifcation of durum wheat with zinc and iron. Cereal Chem. 87, 10-20. doi: 10.1094/CCHEM-87-1-0010
13. Codex Alimentarius, C. (2010). Codex Alimentarius Commision. Codex Stand. 193, 44.
14. Curie, C., Cassin, G., Couch, D., Divol, F., Higuchi, K., Jean, M. L., et al. (2009). Metal movement within plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann. Bot. 103, 1-11. doi: 10.1093/aob/mcn207
15. Del Rosario, A. R., Briones, V. P., Vidal, A. J., and Juliano, B. O. (1968). Composition and endosperm structure of developing and mature rice kernel. Cereal Chem. 45, 225-235.
16. Dobermann, A., and Fairhurst, T. H. (2000). Nutrient Disorders and Nutrient Management. Philippines: Potash and Phosphate Institute, Canada and International Rice Research Institute.
17. Drakakaki, G., Christou, P., and Stoger, E. (2000). Constitutive expression of soybean ferritin cDNA in transgenic wheat and rice results in increased iron levels in vegetative tissues but not in seeds. Transgenic Res. 9, 445-452. doi: 10.1023/A.1026534009483
18. Du Laing, G., Rinklebe, J., Vandecasteele, B., Meers, E., and Tack, F. M. G. (2009). Trace metal behaviour in estuarine and rivering floodplain soils and sediments: A review. Sci. Total Environ. 407, 3972-3985. doi: 10.1016/j.scitotenv.2008.07.025
19. Eriksson, J. E. (1990). Effect of nitrogen-containing fertilizers on solubility and plant uptake of cadmium. Water Air Soil Pollut. 49, 355-368. doi: 10.1007/BF00507075
20. Fang Y., Wang L, Xin Z, Zhao L., An X., Hu, Q. (2008). Effect of foliar application of zinc, selenium, and iron fertilizers on nutrients concentration and yield of rice grain in China. J. Agric. Food Chem. 56,2079-2084. doi: 10.1021/jf800150z
21. Gao, X., Brown, K. R., Racz, G. J., and Grant, C. A. (2010). Concentration of cadmium in durum wheat as affected by tim, source and placement of nitrogen fertilization under reduced and conventional-tillage mangement. PlantSoil 337, 341-354. doi: 10.1007/s11104-010-0531-y
22. Goto, F., Yoshihara, T., Shigemoto, N., Toki, S., and Takaiwa, F. (1999). Iron fortification of rice seed by the soybean ferritin gene. Nat. Biotechnol. 17,282-286. doi: 10.1038/7029
23. Graham, R. D. (2003). Biofortification: A global challenge. Int. Rice Res. Notes 28, 4-8.
24. Graham, R., Senadhira, D., Beebe, S., Iglesias, C., and Monasterio, I. (1999). Breeding for micronutrient density in edible portions of staple food crops: conventional approaches. Fields Crops Res. 60, 57-80. doi: 10.1016/S0378-4290(98)00133-6
25. Gregorio, G., Senadhira, D., Htut, H., and Graham, R. R. (2000). Breeding for trace mineral density in rice. Food Nutr. Bull. 21, 382-386.
26. Haydon, M. J., and Cobbett, C. S. (2007). Transporters of ligands for essential metal ions in plants. New Phytol. 174, 499-506. doi: 10.1111/j.1469-8137.2007.02051.x
27. He, Q. B., and Singh, B. R. (1993). Plant availablity of cadmium in soils. 1. Extractable cadmium in newly and long term cultivated soils. Acta Agric. Scand. B Soil Plant Sci. 43, 134-141.
28. Higuchi, K., Watanabe, S., Takahashi, M., Kawasaki, S., Nakanishi, H., Nishizawa, N. K., etal. (2001). Nicotianamine synthase gene expression differs in barley and rice under Fe-deficient conditions. Plant J. 25, 159-167. doi: 10.1046/j.1365-313x.2001.00951.x
29. Ishikawa, S., Abe, T., Kuramata, M., Yamaguchi, M., Ando, T., Yamamoto, T., et al. (2010). A major quantitative trait locus for increasing cadmium-specific concentration in rice grain is located on the short arm of chromosome 7. J. Exp. Bot. 61, 923-934. doi: 10.1093/jxb/erp360
30. Ishikawa, S., Ae, N., and Yano, M. (2005). Chromosomal regions with quantitative trait loci controlling cadmium concentration in brown rice (Oryza sativa). New Phytol. 168, 345-350. doi: 10.1111/j.1469-8137.2005.01516.x
31. Ishikawa, S., Ishimaru, Y., Igura, M., Kuramata, M., Abe, T., Senoura, T., et al. (2012). Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc. Natl. Acad. Sci. U.S.A. 109, 19166-19171. doi: 10.1073/pnas.1211132109
32. Ishimaru, Y., Masuda, H., Bashir, K., Inoue, H., Tsukamoto, T., Takahashi, M., et al. (2010). Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J. 62, 379-390. doi: 10.1111/j.1365-313X.2010.04158.x
33. Ishimaru, Y., Takahashi, R., Bashir, K., Shimo, H., Senoura, T., Sugimoto, K., etal. (2012). Characterizing the role ofrice NRAMP5 in manganese, iron and cadmium transport. Sci. Rep. 2, 286. doi: 10.1038/srep00286
34. Johnson, A. A. T., Kyriacou, B., Callahan, D. L., Carruthers, L., Stangoulis, J., Lombi, E., et al. (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. doi: 10.1371/journal.pone.0024476
35. Johnson-Beebout, S. E., Lauren, J. G., and Duxbury, J. M. (2009). Immobilization of zinc fertilizer in flooded soils monitored by adapted DTPA soil test. Commun. SoilSci. Plant Anal. 40, 1842-1861. doi: 10.1080/00103620902896738
36. Karak, T., Das, D. K., and Maiti, D. (2006). Yield and zinc uptake in rice (Oryza sativa) as influenced by sources and times of zinc application. Indian J. Agric. Sci. 76, 346-348.
37. Khalekuzzaman, M., Datta, K., Olival, N., Alam, M. F., Joarder, I., and Datta, S. K. (2006). Stable integration, expression and inheritance of the ferritin gene in transgenic elite indica rice cultivar BR29 with enhanced iron level in the endosperm. Indian J. 5, 26-31.
38. Kim, Y.-Y., Yang, Y.-Y., and Lee, Y. (2002). Pb and Cd uptake in rice roots. Physiol.Plant. 116, 368-372. doi: 10.1034/j.1399-3054.2002.1160312.x
39. Kirk, G. (2004). The Biogeochemistry of Submerged Soils. Chichester Wiley
40. Kobayashi, T., and Nishizawa, N. K. (2012). Iron uptake, translocation, and regulation in higher plants. Annu. Rev. Plant Biol. 63, 131-152. doi: 10.1146/annurev-arplant-042811-105522
41. Kutman, U.B., Yildiz, B., Ceylan Y., Ova, E. A., and Cakmak, I. (2012). Contributions of root uptake and remobilization in wheat depending on post-anthesis zinc availability and nitrogen nutrition. Plant Soil 361, 1-2. doi: 10.1007/s11104-012-1300-x
42. Kutman, U. B., Yildiz, B., Ozturk, L., and Cakmak, I. (2010). Biofortification of durum wheat with zinc through soil and foliar applications of nitrogen. Cereal Chem. 87, 1-9. doi: 10.1094/CCHEM-87-1-0001
43. Lee, S., and An, G. (2009). Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant. CellEnviron. 32,408-416. doi: 10.1111/j.1365-3040.2009.01935.x
44. Lee, S., Chiecko, J. C., Kim, S. A., Walker, E. L., Lee, Y., Guerinot, M. L., and SA An,(2009). Disruption of OsYSL15 leads to iron inefficiencyin rice plants. Plant Physiol. 150, 786-800. doi: 10.1104/pp.109.135418
45. Lee, S., Jeon, U. S., Lee, S. J., Kim, Y.-K., Persson, D. P., Husted, S., et al. (2009b). Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proc. Natl. Acad. Sci. U.S.A. 106, 22014-22019. doi: 10.1073/pnas.09109.50106
46. Lee, S., Jeon, J.-S., and An, G. (2012). Iron homeostasis and fortification in rice. J. Plant Biol. 55, 261-267. doi: 10.1007/s12374-011-0386-7
47. Lee, S., Persson, D. P., Hansen, T. H., Husted, S., Schjoerring, J. K., Kim, Y.-S., et al. (2011). Bio-available zinc in rice seeds is increased by activation tagging of nicotianamine synthase. Plant Biotechnol. J. 9, 865-873. doi: 10.1111/j.1467-7652.2011.00606.x
48. Lucca, P., Hurrell, R., and Potrykus, I. (2002). Fighting iron deficiency anemia with iron-rich rice. J. Am. Coll. Nutr. 21, 184-190. doi: 10.1080/07315724.2002.10719264
49. Mabesa, R. L., Impa, S. M., Grewal, D., and Johnson-Beebout, S. E. (2013). Contrasting grain-Zn response ofbiofortification rice (Oryza sativa L.) breeding lines to foliar Zn application. Field Crops Res. 149, 223-233. doi: 10.1016/j.fcr.2013.05.012
50. Martinez, C., Borrero, J., Taboada, R., Viana, J. L., Neves, P., Narvaez, L., et al. (2010). Rice cultivars with enhanced iron and zinc content to improve human nutrition. Paper Presented at the 28th International Rice Research Conference
51. Hanoi Masuda H., Aung, M. S., and Nishizawa, N. K. (2013). Iron biofortification of rice using different transgenic approaches. Rice6, 40. doi: 10.1186/1939-8433-6-40
52. Masuda, H., Kobayashi, T., Ishimaru, Y., Takahashi, M., Aung, M. S., Nakanishi SA, et al. (2013). Iron-biofortification in rice bythe introduction of three barley genes participated in mugineic acidbiosynthesis with soybean ferritin gene. Front. PlantSci. 4:132. doi: 10.3389/fpls.2013.00132
53. Masuda, H., Ishimaru, Y., Aung, M. S., Kobayashi, T., Kakei, Y., Takahashi, M., et al. (2012). Iron biofortification in rice bythe introduction of multiple genes involved in iron nutrition. Sci. Rep. 2, 1-7. doi: 10.1038/srep00543
54. Masuda, H., Suzuki, M., Morikawa, K. C., Kobayashi, T., Nakanishi, H., Takahashi, M., et al. (2008). Increase in iron and zinc concentrations in rice grains viathe introduction of barley genes involved in phytosiderophore synthesis. Rice 1, 100-108. doi: 10.1007/s12284-008-9007-6
55. Masuda, H., Usuda, K., Kobayashi, T., Ishimaru, Y., Kakei, Y., Takahashi, M., etal. (2009). Overexpression of the barley nicotianamine synthase gene HvNAS1 increases iron and zinc concentrations in rice grains. Rice 2, 155-166. doi: 10.1007/s12284-009-9031-9031
56. Mc Lean, E., Cogswell, M., Egli, I., Wojdyla, D., and de Benoist, B. (2009). Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993-2005. Public Health Nutr. 12, 444-454. doi: 10.1017/S1368980008002401
57. Meharg, A. A., Norton, G., Deacon, C., Williams, P., Adomako, E. E., Price, A., et al. (2013). Variation in rice cadmium related to human exposure. Environ. Sci. Technol. 47, 5613-5618. doi: 10.1021/es400521h
58. Miyadate, H., Adachi, S., Hiraizumi, A., Tezuka, K., Nakazawa, N., Kawamoto, T., et al. (2011). OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice bymediating effluxinto vacuoles. NewPhytol. 189,190-199. doi: 10.1111/j.1469-8137.2010.03459.x
59. Nakanishi, H., Ogawa, I., Ishimaru, Y., Mori, S., and Nishizawa, N. K. (2006). Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci. Plant Nutr. 52, 464-469. doi: 10.1111/j.1747-0765.2006.00055.x
60. Neelamraju, S., MallikarjunaSwamy, B. P., Kaladhar, K., Anuradha, K., Venkatesh- warRao, Y., Batchu, A. K., et al. (2012). Increasing iron and zinc in rice grains using deep water rices and wild species - identifying genomic segments and candidate genes. Qual. Assur. Saf. Crop. Foods 4, 138-138. doi: 10.1111/j.1757-837X.2012.00142.x
61. Norton, G. J., Douglas, A., Lahner, B., Yakubova, E., Guerinot, M. L., Pinson, S. R., et al. (2014). Genome wide association mapping of grain arsenic, copper, molybdenum and zinc in rice (Oryza sativa L.) grown at four international field sites. PLoS ONE 9:e89685. doi: 10.1371/journal.pone.0089685
62. Nozoye, T., Nagasaka, S., Kobayashi, T., Takahashi, M., Sato Y., Sato Y., et al. (2011). Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J. Biol. Chem. 286, 5446-5454. doi: 10.1074/jbc.M110.180026
63. Ogo, Y., Itai, R. N., Kobayashi, T., Aung, M. S., Nakanishi, H., and Nishizawa, N. K. (2011). OsIRO2 is responsible for iron utilization in rice and improves growth and yield in calcareous soil. Plant Mol. Biol. 75, 593-605. doi: 10.1007/s11103-011-9752-6
64. Oliva, N., Chadha-Mohanty, P., Poletti, S., Abrigo, E., Atienza, G., Torrizo, L., et al. (2014). Large-scale production and evaluation of marker-free indica rice IR64 expressing phytoferritin genes. Mol. Breed. 33, 23-37. doi: 10.1007/s11032-013-9931-z
65. Olsen, L. I., and Palmgren, M. G. (2014). Many rivers to cross: the journey of zinc from soil to seed. Front. Plant Sci. 5:30. doi: 10.3389/fpls.2014.00030
66. Paul, S., Ali, N., Datta, S. K., and Datta, K. (2014). Development of an iron- enriched high-yieldings indica rice cultivar by introgression of a high-iron trait from transgenic iron-biofortified rice. Plant Foods Hum. Nutr. 69, 203-208. doi: 10.1007/s11130-014-0431-z
67. Paul, S., Ali, N., Gayen, D., Datta, S. K., and Datta, K. (2012). Molecular breeding of Osfer 2 gene to increase iron nutrition in rice grain. GM Crops Food 3, 310-316. doi: 10.4161/gmcr.22104
68. Phattarakul, N., Rerkasem, B., Li, L., J Wu, L. H. Zou, C. Q. Ram, et al. (2012). Biofortification of rice grain with zinc through zinc fertilization in different countries. PlantSoil 361, 131-141. doi: 10.1007/s11104-012-1211-x
69. Qu, L. Q., Yoshihara, T., Ooyama, A., Goto, F., and Takaiwa, F. (2005). Iron accumulation does not parallel the high expression level of ferritin in transgenic rice seeds. Planta 222, 225-233. doi: 10.1007/s00425-005-1530-8
70. Sasaki, A., Yamaji, N., Yokosho, K., and Ma, J. F. (2012). Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24, 2155-2167. doi: 10.1105/tpc.112.096925
71. Satoh-Nagasawa, N., Mori, M., Nakazawa, N., Kawamoto, T., Nagato Y., Sakurai, K., et al. (2012). Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol. 53, 213-224. doi: 10.1093/pcp/pcr166
72. Schmidt, R. J., Tancredi, D. J., Krakowiak, P., Hansen, R. L., and Ozonoff, S. (2014). Maternal intake of supplemental iron and risk of autism spectrum disorder. Am. J. Epidemiol. 180, 890-900. doi: 10.1093/aje/kwu208
73. Singh, B. R. (1990). Uptake of cadmium and fluoride by oat from phosphate fertilizers. Norw J. Agric. Sci. 4, 239-249.
74. Srivastava, P. C., Ghosh, D., and Sing, V. P. (1999). Evaluation of different zinc sources for lowland rice production. Biol. Fert. Soil 30, 168-172. doi: 10.1007/s003740050604
75. Stangoulis, J. C. R., Huynh, B.-L., Welch, R. M., Choi, E.-Y., and Graham, R. D. (2006). Quantitative trait loci for phytate in rice grain and their relationship with grain micronutrient content. Euphytica 154, 289-294. doi: 10.1007/s10681-006-9211-7
76. Stevens, G. A., Finucane, M. M., De-Regil, L. M., Paciorek, C. J., Flaxman, S. R., Branca, F., et al. (2013). Global, regional, and national trends in haemoglobin concentration and prevalence of total and severe anaemia in children and pregnant and non-pregnant women for 1995-2011: A systematic analysis of population-representative data. Lancet Glob. Health 1, e16-e25. doi: 10.1016/S2214-109X(13)70001-9
77. Suzuki, M., Morikawa, K. C., Nakanishi, H., Takahashi, M., Saigusa, M., Mori, S., et al. (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. doi: 10.1111/j.1747-0765.2007.00205.x
78. Takahashi, R., Ishimaru, Y., Senoura, T., Shimo, H., Ishikawa, S., Arao, T., et al. (2011). The OsNRAMP1 iron transporter is involved in Cdaccumulation in rice. J. Exp. Bot. 62, 4843-4850. doi: 10.1093/jxb/err136
79. Takahashi, R., Ishimaru, Y., Shimo, H., Ogo, Y., Senoura, T., Nishizawa, N. K., et al. (2012). The OsHMA2 transporter is involved in root-to-shoottranslocation of Zn and Cd in rice. Plant Cell Environ. 35, 1948-1957. doi: 10.1111/j.1365-3040.2012.02527.x
80. Ueno, D., Yamaji, N., Kono, I., Huang, C. F., Ando, T., Yano, M., et al. (2010). Gene limiting cadmium accumulation in rice. Proc. Natl. Acad. Sci. U.S.A. 107, 16500-16505. doi: 10.1073/pnas.1005396107
81. Uraguchi, S., and Fujiwara, T. (2012). Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice 5, 5. doi: 10.1186/1939-8433-5-5
82. Uraguchi, S., Kamiya, T., Clemens, S., and Fujiwara, T. (2014). Characterization of OsLCT1, a cadmium transporter from indica rice (Oryza sativa). Physiol. Plant. 151, 339-347. doi: 10.1111/ppl.12189
83. Uraguchi, S., Kamiya, T., Sakamoto, T., Kasai, K., Sato, Y., Nagamura, Y., et al. Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proc. Natl. Acad. Sci. U.S.A. 108, 20959-20964. doi: 10.1073/pnas.1116531109
84. Uraguchi, S., Mori, S., Kuramata, M., Kawasaki A., Arao, T., and Ishikawa, S. (2009). Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J. Exp. Bot. 60, 2677-2688. doi: 10.1093/jxb/erp119
85. Vasconcelos, M., Datta, K., Oliva, N., Khalekuzzaman, M., Torrizo, L., Krishnan, S., etal. (2003). Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. PlantSci. 164, 371-378. doi: 10.1016/S0168-9452(02)00421-1
86. Wang, Y., Wei, Y., Dong, L., Lu, L., Feng, Y., Zhang, J., etal. (2014). Improved yield and Zn accumulation for rice grain by Zn fertilization and optimized water management. J. Zhejiang Univ. Sci. B 15, 365-374. doi: 10.1631/jzus.B1300263
87. Wei, Y., Shohag, M. J. I., Yang, X., and Yibin, Z. (2012). Effects of foliar iron application on iron concentration in polished rice grain and its bioavailability. J. Agric. Food Chem. 60, 11433-11439. doi: 10.1021/jf3036462
88. Wei, Y., Shohag, M. J. I., and Yang, X. (2012). Biofortification and bioavailability of rice grain zinc as affected by different forms of foliar Zinc fertilization. PLoS ONE 7:e45428. doi: 10.137/journal.pone.0045428
89. Wessells, K. R., and Brown, K. H. (2012). Estimating the global prevalence of zinc deficiency: results based on zinc availability in national food supplies and the prevalence of stunting. PLoS ONE 7:e50568. doi: 10.1371/journal.pone.0050568
90. Williams, C. H., and David, D. J. (1973). The effect of superphosphate on the Cd content of soils andplants. Aust. J. SoilRes. 11,43-56. doi: 10.1071/SR9730043
91. Wirth, J., Poletti, S., Aeschlimann, B., Yakandawala, N., Drosse, B., Osorio, S., et al. (2009). Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin. Plant Biotechnol. J. 7, 631-644. doi: 10.1111/j.1467-7652.2009.00430.x
92. Wissuwa, M., Ismail, A. M., and Graham, R. D. (2008). Rice grain zinc concentrations as affected by genotype, native soil-zinc availability, and zinc fertilization. PlantSoil 306,37-48.doi: 10.1007/s11104-007-9368-4
93. Zhang, J., Wu, L., and Wang, M. (2008). Can iron and zinc in rice grains (Oryza sativa L.) be biofortified with nitrogen fertilization under pot conditions? J. Sci. FoodAgric. 88, 1172-1177. doi: 10.1002/jsfa.3194
94. Zhang, Y., Xu, Y.-H., Yi, H.-Y., and Gong, J.-M. (2012). Vacuolar membrane transporters OsVIT1 and OsVIT2 modulate iron translocation between flag leaves and seeds in rice. PlantJ. 72,400-410.doi: 10.1111/j.1365-313X.2012.05088.x
95. Zheng, L., Cheng, Z., Ai, C., Jiang, X., Bei X., Zheng, Y., et al. (2010). Nicotianamine, anovel enhancer ofriceironbioavailabilityto humans. PLoS ONE 5:e10190. doi: 10.1371/journal.pone.0010190
96. Zuo Y., and Zhang, F. (2011). Soil and crop management strategies to prevent iron deficiencyin crops. Plant Soil 339, 83-95. doi: 10.1007/s11104-010-0566-0