Iron biofortification of rice using different transgenic approaches

Rice

Volumn 6, Issue 1, 2013, Pages 1-12

  Masuda, Hiroshi ^a   Aung, May Sann ^a   Nishizawa, Naoko K ^a,b  

^a ISHIKAWA PREFECTURAL UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Anemia; Biofortification; Ferritin; IDS3; Iron; Mugineic acids; Nicotianamine; Transgenic rice; YSL; Zinc

Indexed keywords

EID: 84891435868     PISSN: 19398425     EISSN: 19398433     Source Type: Journal    
DOI: 10.1186/1939-8433-6-40     Document Type: Review

References (82)

1. Anuradha K., Agarwal S, Rao YV, Rao KV, Viraktamath BC, Sarla N (2012) Mapping QTLs and candidate genes for iron and zinc concentrations in unpolished rice of Madhukar×Swarna RILs. Gene 508:233-240
2. Aoki N., Hirose T, Scofield NG, Whitfeld RP, Furbank TR (2003) The sucrose transporter gene family in rice. Plant Cell Physiol 44:223-232
3. 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 Mol Biol 70:681-692
4. Aung M.S., Masuda H, Kobayashi T, Nakanishi H, Yamakawa T, Nishizawa NK (2013) Iron biofortification of Myanmar rice. Front Plant Sci 4:158
5. 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. J Biol Chem 281:32395-32402
6. Bashir K., Ishimaru Y, Nishizawa NK (2010) Iron uptake and loading into rice grains. Rice 3:122-130
7. Bashir K., Takahashi R, Akhtar S, Ishimaru Y, Hiromi N, Nishizawa NK (2013) The knockdown of OsVIT2 and MIT2 affects iron localization in rice seed. Rice, 6:31
8. Cesco S., Neumann G, Tomasi N, Pinton R, Weisskopf L (2010) Release of plantborne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329:1-25
9. Curie C., Panavience Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe (III) uptake. Nature 409:346-349
10. Food and Nutrition Board (2001) Dietary reference intakes from vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. Institute of Medicine. National Academic Press, Washington, DC
11. Gómez-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
12. 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
13. Gregorio G.B., Senadhira D, Htut H, Graham RD (2000) Breeding for trace mineral density in rice. Food Nutr Bull 21:382-386
14. Grusak M.A., Cakmak I (2005) Methods to improve the crop delivery of minerals to humans and livestock. In: Broadley MR, White PJ (eds) Plant Nutritional Genomics. Blackwell, Oxford, pp 265-286
15. Grusak M.A., DellaPenna D (1999) Improving the nutrient composition of plants to enhance human nutrition and health. Annu Rev Plant Physiol Plant Mol Biol 50:133-161
16. Haas J.D., Beard JL, Murray-Kolb LE, del Mundo AM, Felix A, Gregorio GB (2005) Iron-biofortified rice improves the iron stores of nonanemic Filipino women. J Nutr 135:2823-2830
17. Hell R., Stephan UW (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216:541-551
18. Higuchi K., Kanazawa K, Nishizawa NK, Chino M, Mori S (1994) Purification and characterization of nicotianamine synthase from Fe-deficient barley roots. Plant Soil 165:173-179
19. Higuchi K., Suzuki K, Nakanishi H, Yamaguchi H, Nishizawa NK, Mori S (1999) Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol 119:471-479
20. Higuchi K., Takahashi M, Nakanishi H, Kawasaki S, Nishizawa NK, Mori S (2001a) Analysis of transgenic rice containing barley nicotianamine synthase gene. Soil Sci Plant Nutr 47:315-322
21. Higuchi K., Watanabe S, Takahashi M, Kawasaki S, Nakanishi H, Nishizawa NK, Mori S (2001b) Nicotianamine synthase gene expression differs in barley and rice under Fe-deficient conditions. Plant J 25:159-167
22. 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 J 36:366-381
23. Inoue H., Takahashi M, Kobayashi T, Suzuki M, Nakanishi H, Mori S, Nishizawa NK (2008) Identification and localization of the rice nicotianamine aminotransferase gene OsNAAT1 expression suggests the site of phytosiderophore synthesis in rice. Plant Mol Biol 66:193-203
24. 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. J Biol Chem 284:3470-3479
25. Ishimaru K., Hirose T, Aoki N, Takahashi S, Ono K, Yamamoto S, Wu J, Saji S, Baba T, Ugaki M, Matsumoto T, Ohsugi R (2001) Antisense expression of a rice sucrose transporter OsSUT1 in rice (Oryza sativa L.). Plant Cell Physiol 42:1181-1185
26. Ishimaru Y., Masuda H, Bashir K, Inoue H, Tsukamoto T, Takahashi M, Nakanishi H, Aoki N., Hirose T, Ohsugi R, Nishizawa NK (2010) Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J 62:379-390
27. 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. J Biol Chem 286:24649-24655
28. Jeng T.L., Lin YW, Wang CS, Sung JM (2012) Comparisons and selection of rice mutants with high iron and zinc contents in their polished grains that were mutated from the indica type cultivar IR64. J Food Compos Anal 28:149-154
29. Johnson A.A.T., Kyriacou B, 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
30. Juliano BS (1993) Rice In Human Nutrition. IRRI, Los Banos
31. Kakei Y., Yamaguchi I, Kobayashi T, Takahashi M, Nakanishi H, Yamakawa T, Nishizawa NK (2009) A highly sensitive, quick and simple quantification method for nicotianamine and 2'-deoxymugineic acid from minimum samples using LC/ESI-TOF-MS achieves functional analysis of these components in plants. Plant Cell Physiol 50:1988-1993
32. Kakei Y., Ishimaru Y, Kobayashi T, Yamakawa T, Nakanishi H, Nishizawa NK (2012) OsYSL16 plays a role in the allocation of iron. Plant Mol Biol 79:583-594
33. Kim S.A., Punshon T, Lanzirotti A, Li L, Alonso JM, Ecker JR, Kaplan J, Guerinot ML (2006) Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314:1295-1298
34. Kobayashi T., Nishizawa NK (2012) Iron Uptake Translocation and Regulation in Higher Plants. Annu Rev Plant Biol 63:131-52
35. Kobayashi T., Nakanishi H, Takahashi M, Kawasaki S, Nishizawa NK, 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
36. 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. Plant J 39:415-424
37. Lee S., An G (2009a) Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant Cell Environ 32:408-416
38. Lee S., Chiecko JC, Kim SA, Walker EL, Lee Y, Guerinot ML, An G (2009b) Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol 150:786-800
39. Lee S., Jeon US, Lee SJ, Kim YK, Persson DP, Husted S, Schjørring JK, Kakei Y, Masuda H., Nishizawa NK, An G (2009c) Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proc Natl Acad Sci USA 106:22014-22019
40. Lonnerdal B (2009) Soybean ferritin: implications for iron status of vegetarians. Am J Clin Nut 89:1680S-1685S
41. Lucca P., Hurrell R, Potrykus I (2002) Fighting iron deficiency anemia with iron-rich rice. J Am Coll Nutr 21:184-190
42. Maclean J.L., Dawe DC, Hardy B, Hettel GP (eds) (2002) Rice almanac, third edition, source book for the most important economic activity on earth. CABI Publishing, Oxfordshire
43. Masuda H., Suzuki M, Morikawa KC, Kobayashi T, Nakanishi H, Takahashi M, Saigusa M., Mori S, Nishizawa NK (2008) Increase in iron and zinc concentrations in rice grains via the introduction of barley genes involved in phytosiderophore synthesis. Rice 1:100-108
44. Masuda H., Usuda K, Kobayashi T, Ishimaru Y, Kakei Y, Takahashi M, Higuchi K, Nakanishi H., Mori S, Nishizawa NK (2009) Overexpression of the barley nicotianamine synthase gene HvNAS1 increase iron and zinc concentrations in rice grains. Rice 2:155-166
45. Masuda H., Ishimaru Y, Aung MS, Kobayashi T, Kakei Y, Takahashi M, Higuchi K, Nakanishi H., Nishizawa NK (2012) Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition. Sci Rep 2:534
46. Masuda H., Kobayashi T, Ishimaru Y, Takahashi M, Aung MS, Nakanishi H, Mori S, Nishizawa NK (2013) Iron-biofortification in rice by the introduction of three barley genes participated in mugineic acid biosynthesis with soybean ferritin gene. Front Plant Sci 4:132
47. Mayer J.E., Pfeiffer WH, Beyer P (2008) Biofortified crops to alleviate micronutrient malnutrition. Curr Opin Plant Biol 11:166-170
48. Mihashi S., Mori S (1989) Characterization of mugineic acid-Fe transporter in Fe-deficient barley roots using the multicompartment transport box method. Biol Met 2:164-154
49. MOH (2003) National Haemoglobin Survey. National plan of action for food and nutrition 2006-2010. Nutrition Section, Department of Health, Ministry of Health (MOH), Yangon
50. Mori S., Nishizawa N (1987) Methionine as a dominant precursor of phytosiderophore in graminaceae plant. Plant Cell Physiol 28:1081-1092
51. 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 Mol Biol 44:199-207
52. Nishiyama R., Kato M, Nagata S, Yanagisawa S, Yoneyama T (2012) Identification of Zn-nicotianamine and Fe-2′-Deoxymugineic acid in the phloem sap from rice plants (Oryza sativa L.). Plant Cell Physiol 53:381-390
53. 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. J Bio Chem 286:5446-5454
54. Ogo Y., Itai RN, Nakanishi H, Inoue H, Kobayashi T, Suzuki M, Takahashi M, Mori S, Nishizawa NK (2006) Isolation and characterization of IRO2, a novel iron-regulated bHLH transcription factor in graminaceous plants. J Exp Bot 57:2867-2878
55. Ogo Y., Itai RN, Nakanishi H, Kobayashi T, Takahashi M, Mori S, Nishizawa NK (2007) The rice bHLH protein OsIRO2 is an essential regulator of the genes involved in Fe uptake under Fe deficient conditions. Plant J 51:366-377
56. Ogo Y., Itai RN, Kobayashi T, Aung MS, Nakanishi H, Nishizawa NK (2011) OsIRO2 is responsible for iron utilization in rice and improves growth and yield in calcareous soil. Plant Mol Biol 75:593-605
57. Paul S., Ali N, Gayen D, Datta SK, Datta K (2012) Molecular breeding of Osfer2 gene to increase iron nutrition in rice grain. GM Crops Food 3:310-316
58. Pfeiffer W.H., Mcclafferty B (2007) HarvestPlus: Breeding crops for better nutrition. Crop Sci 47:S88-S105
59. Pich A., Scholz G (1996) Translocation of copper and other micronutrients in tomato plants (Lycopersicon esculentum Mill.): nicotianamine-stimulated copper transport in the xylem. J Exp Bot 294:41-47
60. Qu L.Q., Yoshihara T, Ooyama A, Goto F, Takaiwa F (2005) Iron accumulation does not parallel the high expression level of ferritin in transgenic rice seeds. Planta 222:225-233
61. Rudolph A., Becker R, Scholz G, Procházka Z, Toman J, Macek T, Herout V (1985) The occurrence of the amino acid nicotianamine in plants and microorganisms: a reinvestigation. Biochemie und Physiologie der Pflanzen 180:557-563
62. Ruengphayak S., Ruanjaichon V, Phromphan S, Chaichumpoo E, Saensuk C, Toojinda T., Tragoonrung S, Kongkachuichai R, Vanavichit A (2012) Reverse and forward genetics approaches to identify mutants conferring high grain Fe density and tolerance to Fe toxicity. Paper presented at the 10th International Symposium on Rice Functional Genomics, Lotus Hotel Pang Suan Kaew, Chiang Mai
63. Schroeder J.I., Delhaize E, Frommer WB, Guerinot ML, Harrison MJ, Herrera-Estrella L, Horie T, Kochian LV, Munns R, Nishizawa NK, Tsay YF, Sanders D (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497:60-66
64. Scofield G.N., Hirose T, Aoki N, Furbank TR (2007) Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice. J Exp Bot 58:3155-3169
65. Sperotto R.A., Boff T, Duarte GL, Santos LS, Grusak MA, Fett JP (2010) Identification of putative target genes to manipulate Fe and Zn concentrations in rice grains. J Plant Physiol 167:1500-1506
66. Stephan U.W., Schmidke I, Stephan VW, Scholz G (1996) The nicotianamine molecule is made-to-measure for complexation of metal micronutrients in plants. Biometals 9:84-90
67. Stoltzfus R.J., Dreyfuss ML (1998) Guidelines for the use of iron supplements to prevent and treat iron deficiency anemia. ILSI Press, Washington DC
68. 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
69. Takagi S (1976) Naturally occurring iron-chelating compounds in oat-and rice-root washings. Soil Sci Plant Nutr 22:423-433
70. Takahashi M., Yamaguchi H, Nakanishi H, Shioiri T, Nishizawa NK, Mori S (1999) Cloning two genes for nicotianamine aminotransferase, a critical enzyme in iron acquisition (Strategy II) in graminaceous plants. Plant Physiol 121:947-956
71. Takahashi M., Nakanishi H, Kawasaki S, Nishizawa NK, Mori S (2001) Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. Nat Biotech 19:466-469
72. 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
73. Takahashi R., Ishimaru Y, Shimo H, Ogo Y, Senoura T, Nishizawa NK, Nakanishi H (2012) The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ 35:1948-1957
74. Theil EC (2003) Ferritin: at the crossroads of iron and oxygen metabolism. J Nutr 133:1549-1553
75. Theil EC (2011) Iron Homeostasis and Nutritional Iron Deficiency. J Nutr 141:724S-728S
76. Theil E.C., Chen H, Miranda C, Janser H, Elsenhans B, Núñez MT, Pizarro F, Schümann K (2012) Absorption of Iron from Ferritin Is Independent of Heme Iron and Ferrous Salts in Women and Rat Intestinal Segments. J Nutr 142:478-483
77. 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
78. von Wirén N, Khodr H, Hider RC (2000) Hydroxylated phytosiderophore species from rye and barley possess an enhanced chelating efficiency and affinity for iron(III). Plant Physiol 124:1149-1157
79. Wang M., Gruissem W, Bhullar NK (2013) Nicotianamine synthase overexpression positively modulates iron homeostasis-related genes in high iron rice. Front Plant Sci 4:156. doi:10.3389/fpls.2013.00156
80. WHO (2002) The World Health Report. Reducing Risks, Promoting Healthy Life. Word Health Organization (WHO), Geneva
81. Wirth J., Poletti S, Aeschlimann B, Yakandawala N, Drosse B, Osorio S, Tohge T, Fernie A.R., Günther D, Gruissem W, Sautter C (2009) Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin. Plant Biotech J 7:1-14
82. Zhang Y., Xu YH, Yi HY, Gong JM (2012) Vacuolar membrane transporters OsVIT1 and OsVIT2 modulate iron translocation between flag leaves and seeds in rice. Plant J 72:400-410