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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Enhancing the chelation capacity of rice to maximise iron and zinc concentrations under elevated atmospheric carbon dioxide

Alexander A. T. Johnson
+ Author Affiliations
- Author Affiliations

School of Botany, The University of Melbourne, Parkville, Vic. 3010; Australian Centre for Plant Functional Genomics, University of Adelaide, PMB1, Glen Osmond, SA 5064, Australia. Email: johnsa@unimelb.edu.au

Functional Plant Biology 40(2) 101-108 https://doi.org/10.1071/FP12029
Submitted: 25 January 2012  Accepted: 27 March 2012   Published: 11 May 2012

Abstract

Roughly half of the Earth’s seven billion people rely on rice as their primary source of food. The milled grain of rice, often referred to as polished or white rice, serves as a rich source of energy but is low in protein and several essential micronutrients such as iron and zinc. As a result, billions of people in rice-based countries suffer the debilitating effects of protein-energy and micronutrient malnutrition with symptoms including iron-deficiency anaemia, growth retardation and blindness. By 2050, the Earth’s atmospheric carbon dioxide concentration ([CO2]) is expected to reach 550 μmol mol–1, representing a 70% increase from today’s concentration of 392 μmol mol–1. The impacts of elevated [CO2] on plant growth will likely include agronomically useful traits such as increased biomass, yield and water-use efficiency. However, increased plant productivity is likely to be accompanied by decreased protein and micronutrient mineral concentrations of cereal grain. This review focuses on the effects of carbon dioxide-enrichment on rice physiology and nutritional composition and proposes increased activity of the Strategy II iron uptake pathway as a promising method to maintain or increase iron and zinc concentrations in rice grain, and perhaps cereal grain in general, under elevated [CO2].

Additional keywords: biofortification, FACE, hidden hunger, nicotianamine, phytate, Strategy II.


References

Ainsworth EA (2008) Rice production in a changing climate: a meta-analysis of responses to elevated carbon dioxide and elevated ozone concentration. Global Change Biology 14, 1642–1650.
Rice production in a changing climate: a meta-analysis of responses to elevated carbon dioxide and elevated ozone concentration.Crossref | GoogleScholarGoogle Scholar |

Ainsworth EA, McGrath JM (2010) Direct effects of rising atmospheric carbon dioxide and ozone on crop yields. In ‘Cimate change and rood security – adopting agriculture to a warmer world’. (Eds D Lobell, M Burke) pp. 109–130. (Springer-Verlag: Dordrecht, The Netherlands)

Arsenault JE, Yakes EA, Hossain MB, Islam MM, Ahmed T, Hotz C, Lewis B, Rahman AS, Jamil KM, Brown KH (2010) The current high prevalence of dietary zinc inadequacy among children and women in rural Bangladesh could be substantially ameliorated by zinc biofortification of rice. Journal of Nutrition 140, 1683–1690.
The current high prevalence of dietary zinc inadequacy among children and women in rural Bangladesh could be substantially ameliorated by zinc biofortification of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFajurbK&md5=312d0453d8a2753b4905ca4f4ff839a6CAS |

Bouis HE, Hotz C, McClafferty B, Meenakshi JV, Pfeiffer WH (2011) Biofortification: a new tool to reduce micronutrient malnutrition. Food and Nutrition Bulletin 32, 31S–40S.

Cassin G, Mari S, Curie C, Briat J-F, Czernic P (2009) Increased sensitivity to iron deficiency in Arabidopsis thaliana overaccumulating nicotianamine. Journal of Experimental Botany 60, 1249–1259.
Increased sensitivity to iron deficiency in Arabidopsis thaliana overaccumulating nicotianamine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFShsLY%3D&md5=bdb33c2c441938da68ab87da40225eaeCAS |

Cheng W, Sakai H, Yagi K, Hasegawa T (2009) Interactions of elevated [CO2] and night temperature on rice growth and yield. Agricultural and Forest Meteorology 149, 51–58.
Interactions of elevated [CO2] and night temperature on rice growth and yield.Crossref | GoogleScholarGoogle Scholar |

Conroy JP, Seneweera S, Basra AS, Rogers G, Nissen-Wooller B (1994) Influence of rising atmospheric CO2 concentrations and temperature on growth, yield and grain quality of cereal crops. Functional Plant Biology 21, 741–758.

de Onis M, Monteiro C, Akré J, Clugston G (1993) The worldwide magnitude of protein-energy malnutrition: an overview from the WHO Global Database on Child Growth. Bulletin of the World Health Organization 71, 703–712.

Erbs M, Manderscheid R, Jansen G, Seddig S, Pacholski A, Weigel H-J (2010) Effects of free-air CO2 enrichment and nitrogen supply on grain quality parameters and elemental composition of wheat and barley grown in a crop rotation. Agriculture Ecosystems & Environment 136, 59–68.
Effects of free-air CO2 enrichment and nitrogen supply on grain quality parameters and elemental composition of wheat and barley grown in a crop rotation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGrsr8%3D&md5=22635df782d7fb8c6eff34a50b95357bCAS |

Food and Agricultural Organization of the United Nations (FAO) (2006) ‘World agriculture: towards 2030/2050. Interim Report.’ (Global Perspective Studies Unit, Food and Agriculture Organization of the United Nations: Rome)

Högy P, Fangmeier A (2008) Effects of elevated atmospheric CO2 on grain quality of wheat. Journal of Cereal Science 48, 580–591.
Effects of elevated atmospheric CO2 on grain quality of wheat.Crossref | GoogleScholarGoogle Scholar |

Hurrell RF (2003) Influence of vegetable protein sources on trace element and mineral bioavailability. Journal of Nutrition 133, 2973S–2977S.

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 Journal 36, 366–381.
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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVykurc%3D&md5=8e3e0b67a8a1a3e2c82f22364c35a358CAS |

Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa NK (2008) 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. Journal of Biological Chemistry 284, 3470–3479.
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.Crossref | GoogleScholarGoogle Scholar |

Johnson AAT, 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
Constitutive overexpression of the OsNAS gene family reveals single-gene strategies for effective iron- and zinc-biofortification of rice endosperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1entLzO&md5=b8fd249abebc06f02efbb3d1ee42cdecCAS |

Juliano BO (1993) Rice in human nutrition. FAO Food and Nutrition Series No. 26. Food and Agriculture Organization of the United Nations and International Rice Research Institute, Rome.

Kennedy G, Burlingame B (2003) Analysis of food composition data on rice from a plant genetic resources perspective. Food Chemistry 80, 589–596.
Analysis of food composition data on rice from a plant genetic resources perspective.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosV2jtQ%3D%3D&md5=e499b6e38d552483b91fa234470d11ffCAS |

Kimball BA, Morris CF, Pinter PJ, Wall GW, Hunsaker DJ, Adamsen FJ, LaMorte RL, Leavitt SW, Thompson TL, Matthias AD, Brooks TJ (2001) Elevated CO2, drought and soil nitrogen effects on wheat grain quality. New Phytologist 150, 295–303.
Elevated CO2, drought and soil nitrogen effects on wheat grain quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvVegsro%3D&md5=daa068f9c23c21cb98a26c75760131e6CAS |

Klatte M, Schuler M, Wirtz M, Fink-Straube C, Hell R, Bauer P (2009) The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiology 150, 257–271.
The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFahs7o%3D&md5=034604ff6c206b9124e7a63753c2e9d8CAS |

Kobayashi T, Ogo Y, Itai RN, Nakanishi H, Takahashi M, Mori S, Nishizawa NK (2007) The transcription factor IDEF1 regulates the response to and tolerance of iron deficiency in plants. Proceedings of the National Academy of Sciences of the United States of America 104, 19 150–19 155.
The transcription factor IDEF1 regulates the response to and tolerance of iron deficiency in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSksLvL&md5=23df3df3d6c15dc481faf50516d34bcaCAS |

Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. Journal of Experimental Botany 60, 2859–2876.
Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFWjtLc%3D&md5=00ad27ce896a57ced33eabbe90fd634eCAS |

Lee S, Jeon US, Lee SJ, Kim Y-K, Persson DP, Husted S, Schjørring JK, Kakei Y, Masuda H, Nishizawa NK, Ana G (2009) Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proceedings of the National Academy of Sciences of the United States of America 106, 22 014–22 019.
Iron fortification of rice seeds through activation of the nicotianamine synthase gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltlCmsg%3D%3D&md5=11a0741f2b88a6623f9535e09bcc6804CAS |

Lee S, Persson DP, Hansen TH, Husted S, Schjoerring JK, Kim Y-S, Jeon US, Kim Y-K, Kakei Y, Masuda H, Nishizawa NK, An G (2011) Bio-available zinc in rice seeds is increased by activation tagging of nicotianamine synthase. Plant Biotechnology Journal 9, 865–873.
Bio-available zinc in rice seeds is increased by activation tagging of nicotianamine synthase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlemtrjE&md5=1b2bba2195e78b841ffbcf2c82ea45deCAS |

Lee S, Kim Y-S, Jeon U, Kim Y-K, Schjoerring J, An G (2012) Activation of rice nicotianamine synthase 2 (OsNAS2) enhances iron availability for biofortification. Molecules and Cells 33, 269–275.

Lieffering M, Kim H-Y, Kobayashi K, Okada M (2004) The impact of elevated CO2 on the elemental concentrations of field-grown rice grains. Field Crops Research 88, 279–286.
The impact of elevated CO2 on the elemental concentrations of field-grown rice grains.Crossref | GoogleScholarGoogle Scholar |

Loladze I (2002) Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry? Trends in Ecology & Evolution 17, 457–461.
Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry?Crossref | GoogleScholarGoogle Scholar |

Long SP, Ainsworth EA, Leakey ADB, Nösberger J, Ort DR (2006) Food for thought: lower-than-expected crop yield stimulation with rising CO2 concentrations. Science 312, 1918–1921.
Food for thought: lower-than-expected crop yield stimulation with rising CO2 concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmsVagsr4%3D&md5=b38db44b92d6b5bb33835b981de72201CAS |

Lucca P, Hurrell R, Potrykus I (2002) Fighting iron deficiency anemia with iron-rich rice. Journal of the American College of Nutrition 21, 184S–190S.

Ma JF (2005) Plant root responses to three abundant soil minerals: silicon, aluminum and iron. Critical Reviews in Plant Sciences 24, 267–281.
Plant root responses to three abundant soil minerals: silicon, aluminum and iron.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtV2gsr7K&md5=d0c0395f07431b8152b8c134e1270194CAS |

Mahmoud AA, Sukumar S, Krishnan HB (2008) Interspecific rice hybrid of Oryza sativa × Oryza nivara reveals a significant increase in seed protein content. Journal of Agricultural and Food Chemistry 56, 476–482.
Interspecific rice hybrid of Oryza sativa × Oryza nivara reveals a significant increase in seed protein content.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntVGm&md5=605788242be6d7523e71b1c9f4728d76CAS |

Manderscheid R, Bender J, Jäger HJ, Weigel HJ (1995) Effects of season long CO2 enrichment on cereals. II. Nutrient concentrations and grain quality. Agriculture Ecosystems & Environment 54, 175–185.
Effects of season long CO2 enrichment on cereals. II. Nutrient concentrations and grain quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXoslKhs78%3D&md5=8903f31e1d4c5a40947eaf1d13ba6441CAS |

Manoj-Kumar (2011) Will rising CO2 affect Zn and Fe bioavailability in food grains? Current Science 101, 467

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 increases iron and zinc concentrations in rice grains. Rice 2, 155–166.
Overexpression of the barley nicotianamine synthase gene HvNAS1 increases iron and zinc concentrations in rice grains.Crossref | GoogleScholarGoogle Scholar |

Mayer JE, Pfeiffer WH, Beyer P (2008) Biofortified crops to alleviate micronutrient malnutrition. Current Opinion in Plant Biology 11, 166–170.
Biofortified crops to alleviate micronutrient malnutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktFCms7s%3D&md5=9c810f818627eeafebd1d36139685ac6CAS |

Mizuno D, Higuchi K, Sakamoto T, Nakanishi H, Mori S, Nishizawa NK (2003) Three nicotianamine synthase genes isolated from maize are differentially regulated by iron nutritional status. Plant Physiology 132, 1989–1997.
Three nicotianamine synthase genes isolated from maize are differentially regulated by iron nutritional status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsVantL0%3D&md5=c96bc324add66b70f415c7a1778f74bcCAS |

Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2010) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. Journal of Biological Chemistry 286, 5446–5454.
Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants.Crossref | GoogleScholarGoogle Scholar |

Ogo Y, Nakanishi Itai R, 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. The Plant Journal 51, 366–377.
The rice bHLH protein OsIRO2 is an essential regulator of the genes involved in Fe uptake under Fe-deficient conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVKjurk%3D&md5=41673099e1b81e967f990c4e72c53fa7CAS |

Pal M, Rao LS, Srivastava AC, Jain V, Sengupta UK (2003) Impact of CO2 enrichment and variable nitrogen supplies on composition and partitioning of essential nutrients of wheat. Biologia Plantarum 47, 227–231.
Impact of CO2 enrichment and variable nitrogen supplies on composition and partitioning of essential nutrients of wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkslemtA%3D%3D&md5=021d2b1d435b285f992f2e1713cc5625CAS |

Pang J, Zhu J-G, Xie Z-B, Liu G, Zhang Y-L, Chen G-P, Zeng Q, Cheng L (2006) A new explanation of the N concentration decrease in tissues of rice (Oryza sativa L.) exposed to elevated atmospheric pCO2. Environmental and Experimental Botany 57, 98–105.
A new explanation of the N concentration decrease in tissues of rice (Oryza sativa L.) exposed to elevated atmospheric pCO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkslSks7Y%3D&md5=a79ba1002ea334feca91d6370eaf1f20CAS |

Ramakrishnan U (2002) Prevalence of micronutrient malnutrition worldwide. Nutrition Reviews 60, S46–S52.
Prevalence of micronutrient malnutrition worldwide.Crossref | GoogleScholarGoogle Scholar |

Seneweera S, Blakeney A, Milham P, Basra AS, Barlow EWR, Conroy J (1996) Influence of rising atmospheric CO2 and phosphorus nutrition on the grain yield and quality of rice (Oryza sativa cv. Jarrah). Cereal Chemistry 73, 239–243.

Seneweera SP, Conroy JP (1997) Growth, grain yield and quality of rice (Oryza sativa L.) in response to elevated CO2 and phosphorus nutrition. Soil Science and Plant Nutrition 43, 1131–1136.

Suzuki M, Morikawa KC, Nakanishi H, Takahashi M, Saigusa M, Mori S, Nishizawa NK (2008a) Transgenic rice lines that include barley genes have increased tolerance to low iron availability in a calcareous paddy soil. Soil Science and Plant Nutrition 54, 77–85.
Transgenic rice lines that include barley genes have increased tolerance to low iron availability in a calcareous paddy soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjt1Whsbk%3D&md5=4fc22be11243e888ec74f7a2eb49b528CAS |

Suzuki M, Tsukamoto T, Inoue H, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2008b) Deoxymugineic acid increases Zn translocation in Zn-deficient rice plants. Plant Molecular Biology 66, 609–617.
Deoxymugineic acid increases Zn translocation in Zn-deficient rice plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsFWlsr0%3D&md5=07360d14c8681300a69a085c06800fd2CAS |

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. Nature Biotechnology 19, 466–469.
Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtlOktbY%3D&md5=dbe88cb03d3a55ab1e8a35e607922facCAS |

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. The Plant Cell 15, 1263–1280.
Role of nicotianamine in the intracellular delivery of metals and plant reproductive development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvVeksbo%3D&md5=5d22fefabaafb1db63ed6c79dbfc5beeCAS |

Takemoto T, Nomoto K, Fushiya S, Ouchi R, Kusano G, Hikino H, Takagi S-i, Matsuura Y, Kakudo M (1978) Structure of mugineic acid, a new amino acid possessing an iron-chelating activity from roots washings of water-cultured Hordeum vulgare L. Proceedings of the Japan Academy 54, 469–473.
Structure of mugineic acid, a new amino acid possessing an iron-chelating activity from roots washings of water-cultured Hordeum vulgare L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXot1Citg%3D%3D&md5=cff50633a599b046667ed6bb571c13ecCAS |

Taub DR, Wang X (2008) Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses. Journal of Integrative Plant Biology 50, 1365–1374.
Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVyltb7M&md5=0dcf3a7b71f228f6539ab2ba9540b053CAS |

Taub DR, Miller B, Allen H (2008) Effects of elevated CO2 on the protein concentration of food crops: a meta-analysis. Global Change Biology 14, 565–575.
Effects of elevated CO2 on the protein concentration of food crops: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Terao T, Miura S, Yanagihara T, Hirose T, Nagata K, Tabuchi H, Kim H-Y, Lieffering M, Okada M, Kobayashi K (2005) Influence of free-air CO2 enrichment (FACE) on the eating quality of rice. Journal of the Science of Food and Agriculture 85, 1861–1868.
Influence of free-air CO2 enrichment (FACE) on the eating quality of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXosVentLc%3D&md5=d4f6fbf16d5b1d1234018273cf062767CAS |

United Nations, Department of Economic and Social Affairs, Population Division (2009) World Population Prospects: the 2008 Revision, Highlights, Working Paper No. ESA/P/WP.210.

von Braun J, Bos MS (2005) The changing economics and politics of rice: implications for food security, globalization and environmental sustainability. In ‘Rice is life: scientific perspectives for the 21st century’. (Eds K Toriyama, KL Heong, B Hardy) pp. 7–20. (International Rice Research Institute (IRRI): Los Baños, Philippines)

von Wirén N, Klair S, Bansal S, Briat J-F, Khodr H, Shioiri T, Leigh RA, Hider RC (1999) Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants. Plant Physiology 119, 1107–1114.
Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants.Crossref | GoogleScholarGoogle Scholar |

Wang Y, Frei M, Song Q, Yang L (2011) The impact of atmospheric CO2 concentration enrichment on rice quality – a research review. Acta Ecologica Sinica 31, 277–282.
The impact of atmospheric CO2 concentration enrichment on rice quality – a research review.Crossref | GoogleScholarGoogle Scholar |

Wirth J, Poletti S, Aeschlimann B, Yakandawala N, Drosse B, Osorio S, Tohge T, Fernie AR, Günther D, Gruissem W, Sautter C (2009) Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin. Plant Biotechnology Journal 7, 631–644.
Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFeqtLvO&md5=965e64da54ab0e0546df673c8b3a4f75CAS |

Yang L, Huang J, Yang H, Zhu J, Liu H, Dong G, Liu G, Han Y, Wang Y (2006) The impact of free-air CO2 enrichment (FACE) and N supply on yield formation of rice crops with large panicle. Field Crops Research 98, 141–150.
The impact of free-air CO2 enrichment (FACE) and N supply on yield formation of rice crops with large panicle.Crossref | GoogleScholarGoogle Scholar |

Ye X, Al-Babili S, Klöti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287, 303–305.
Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvVWqtw%3D%3D&md5=1d93ff95ae6b7616580f00c4b9a6e03fCAS |

Zheng L, Cheng Z, Ai C, Jiang X, Bei X, Zheng Y, Glahn RP, Welch RM, Miller DD, Lei XG, Shou H (2010a) Nicotianamine, a novel enhancer of rice iron bioavailability to humans. PLoS ONE 5, e10190
Nicotianamine, a novel enhancer of rice iron bioavailability to humans.Crossref | GoogleScholarGoogle Scholar |

Zheng L, Ying Y, Wang L, Wang F, Whelan J, Shou H (2010b) Identification of a novel iron regulated basic helix-loop-helix protein involved in Fe homeostasis in Oryza sativa. BMC Plant Biology 10, 166
Identification of a novel iron regulated basic helix-loop-helix protein involved in Fe homeostasis in Oryza sativa.Crossref | GoogleScholarGoogle Scholar |