Biofortification of iron and zinc in rice and wheat.
biofortification
hidden hunger
iron and zinc deficiency
malnutrition
micronutrient
rice
wheat
Journal
Journal of integrative plant biology
ISSN: 1744-7909
Titre abrégé: J Integr Plant Biol
Pays: China (Republic : 1949- )
ID NLM: 101250502
Informations de publication
Date de publication:
Jun 2022
Jun 2022
Historique:
received:
09
03
2022
accepted:
08
04
2022
pubmed:
10
4
2022
medline:
16
6
2022
entrez:
9
4
2022
Statut:
ppublish
Résumé
Iron and zinc are critical micronutrients for human health. Approximately two billion people suffer from iron and zinc deficiencies worldwide, most of whom rely on rice (Oryza sativa) and wheat (Triticum aestivum) as staple foods. Therefore, biofortifying rice and wheat with iron and zinc is an important and economical approach to ameliorate these nutritional deficiencies. In this review, we provide a brief introduction to iron and zinc uptake, translocation, storage, and signaling pathways in rice and wheat. We then discuss current progress in efforts to biofortify rice and wheat with iron and zinc. Finally, we provide future perspectives for the biofortification of rice and wheat with iron and zinc.
Substances chimiques
Iron
E1UOL152H7
Zinc
J41CSQ7QDS
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1157-1167Subventions
Organisme : National Natural Science Foundation of China
Organisme : Talents Program of Jiangxi Province
Informations de copyright
© 2022 Institute of Botany, Chinese Academy of Sciences.
Références
Aggett, P.J. (2020). Chapter 22 - Iron. In: Marriott, B.P., Birt, D.F., Stallings, V.A., and Yates, A.A. eds, Present Knowledge in Nutrition (Eleventh Edition), Academic Press, London, UK. pp. 375-392.
Aoyama, T., Kobayashi, T., Takahashi, M., Nagasaka, S., Usuda, K., Kakei, Y., Ishimaru, Y., Nakanishi, H., Mori, S., and Nishizawa, N.K. (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.
Babu, P.M., Neeraja, C.N., Rathod, S., Suman, K., Uttam, G.A., Chakravartty, N., Lachagari, V.B.R., Chaitanya, U., Rao, L.V.S., and Voleti, S.R. (2020). Stable SNP allele associations with high grain zinc content in polished rice (Oryza sativa L.) identified based on ddRAD sequencing. Front. Genet. 11: 763.
Bashir, K., Inoue, H., Nagasaka, S., Takahashi, M., Nakanishi, H., Mori, S., and Nishizawa, N.K. (2006). Cloning and characterization of deoxymugineic acid synthase genes from graminaceous plants. J. Biol. Chem. 281: 32395-32402.
Borg, S., Brinch-Pedersen, H., Tauris, B., Madsen, L.H., Darbani, B., Noeparvar, S., and Holm, P.B. (2012). Wheat ferritins: Improving the iron content of the wheat grain. J. Cereal Sci. 56: 204-213.
Bouis, H.E., Hotz, C., McClafferty, B., Meenakshi, J.V., and Pfeiffer, W.H. (2011). Biofortification: A new tool to reduce micronutrient malnutrition. Food. Nutr. Bull. 32: S31-S40.
Brier, N., Gomand, S.V., Donner, E., Paterson, D., Delcour, J.A., Lombi, E., and Smolders, E. (2015). Distribution of minerals in wheat grains (Triticum aestivum L.) and in roller milling fractions affected by pearling. J. Agric. Food Chem. 63: 1276-1285.
Bughio, N., Yamaguchi, H., Nishizawa, N.K., Nakanishi, H., and Mori, S. (2002). Cloning an iron-regulated metal transporter from rice. J. Exp. Bot. 53: 1677-1682.
Cai, H., Huang, S., Che, J., Yamaji, N., and Ma, J.F. (2019). The tonoplast-localized transporter OsHMA3 plays an important role in maintaining Zn homeostasis in rice. J. Exp. Bot. 70: 2717-2725.
Curie, C., Panaviene, Z., Loulergue, C., Dellaporta, S.L., Briat, J.F., and Walker, E.L. (2001). Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409: 346-349.
Che, J., Yamaji, N., and Ma, J.F. (2021). Role of a vacuolar iron transporter OsVIT2 in the distribution of iron to rice grains. New Phytol. 230: 1049-1062.
Cheng, L., Wang, F., Shou, H., Huang, F., Zheng, L., He, F., Li, J., Zhao, F.J., Ueno, D., Ma, J.F., and Wu, P. (2007). Mutation in nicotianamine aminotransferase stimulated the Fe(II) acquisition system and led to iron accumulation in rice. Plant Physiol. 145: 1647-1657.
Connorton, J.M., Jones, E.R., Rodriguez-Ramiro, I., Fairweather-Tait, S., Uauy, C., and Balk, J. (2017). Wheat vacuolar iron transporter TaVIT2 transports Fe and Mn and is effective for biofortification. Plant Physiol. 174: 2434-2444.
Crespo-Herrera, L.A., Govindan, V., Stangoulis, J., Hao, Y., and Singh, R.P. (2017). QTL mapping of grain Zn and Fe concentrations in two hexaploid wheat RIL populations with ample transgressive segregation. Front. Plant Sci. 8: 1800.
Curie, C., Cassin, G., Couch, D., Divol, F., Higuchi, K., Le Jean, M., Misson, J., Schikora, A., Czernic, P., and Mari, S. (2009). Metal movement within the plant: Contribution of nicotianamine and yellow stripe 1-like transporters. Ann. Bot. 103: 1-11.
Descalsota, G.I.L., Swamy, B.P.M., Zaw, H., Inabangan-Asilo, M.A., Amparado, A., Mauleon, R., Chadha-Mohanty, P., Arocena, E.C., Raghavan, C., Leung, H., Hernandez, J.E., Lalusin, A.B., Mendioro, M.S., Diaz, M.G.Q., and Reinke, R. (2018). Genome-wide association mapping in a rice MAGIC plus population detects QTLs and genes useful for biofortification. Front. Plant Sci. 9: 1347.
Deshpande, P., Dapkekar, A., Oak, M.D., Paknikar, K.M., and Rajwade, J.M. (2017). Zinc complexed chitosan/TPP nanoparticles: A promising micronutrient nanocarrier suited for foliar application. Carbohydr. Polym. 165: 394-401.
Doolette, C.L., Read, T.L., Howell, N.R., Cresswell, T., and Lombi, E. (2020). Zinc from foliar-applied nanoparticle fertiliser is translocated to wheat grain: A (65) Zn radiolabelled translocation study comparing conventional and novel foliar fertilisers. Sci. Total Environ 749: 142369.
Fakharzadeh, S., Hafizi, M., Baghaei, M.A., Etesami, M., Khayamzadeh, M., Kalanaky, S., Akbari, M.E., and Nazaran, M.H. (2020). Using nanochelating technology for biofortification and yield increase in rice. Sci. Rep. 10: 4351.
Fitzgerald, M.A., McCouch, S.R., and Hall, R.D. (2009). Not just a grain of rice: The quest for quality. Trends Plant Sci. 14: 133-139.
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.
Grahama, R., Senadhira, D., Beebe, S., Iglesias, C., and Monasterio, I. (1999). Breeding for micronutrient density in edible portions of staple food crops conventional approaches. Field Crops Res. 60: 57-80.
Grebmer, K., Saltzman, A., Birol, E., Wiesmann, D., Prasai, N., Yin, S., Yohannes, Y., Menon, P., Thompson, J., and Sonntag, A. (2014). 2014 global hunger index: The challenge of hidden hunger. International Food Policy Research Institute, Welthungerhilfe, and Concern Worldwide.
Guo, M., Ruan, W., Zhang, Y., Zhang, Y., Wang, X., Guo, Z., Wang, L., Zhou, T., Paz-Ares, J., and Yi, K. (2022). A reciprocal inhibitory module for Pi and iron signaling. Mol. Plant 15: 138-150.
Gyani, P.C., Bollinedi, H., Gopala Krishnan, S., Vinod, K.K., Sachdeva, A., Bhowmick, P.K., Ellur, R.K., Nagarajan, M., Singh, A.K. (2020). Genetic analysis and molecular mapping of the quantitative trait loci governing low phytic acid content in a novel LPA rice mutant, PLM11. Plants (Basel). 9: 1728.
Hensawang, S., Lee, B.T., Kim, K.W., and Chanpiwat, P. (2020). Probabilistic assessment of the daily intake of microelements and toxic elements via the consumption of rice with different degrees of polishing. J. Sci. Food Agric. 100: 4029-4039.
Higuchi, K., Suzuki, K., Nakanishi, H., Yamaguchi, H., Nishizawa, N.-K., and Mori, S. (1999). Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol. 119: 471-480.
Huang, S., Sasaki, A., Yamaji, N., Okada, H., Mitani-Ueno, N., and Ma, J.F. (2020a). The ZIP transporter family member OsZIP9 contributes to root zinc uptake in rice under zinc-limited conditions. Plant Physiol. 183: 1224-1234.
Huang, S., Wang, P., Yamaji, N., and Ma, J.F. (2020b). Plant nutrition for human nutrition: Hints from rice research and future perspectives. Mol. Plant 13: 825-835.
Ishida, Y., Hiei, Y., and Komari, T. (2015). High efficiency wheat transformation mediated by agrobacterium tumefaciens. In Ogihara, Y., Takumi, S., Handa, H. eds. Advances in Wheat Genetics: From Genome to Field, Tokyo, Springer, pp. 167-173.
Ishikawa, R., Iwata, M., Taniko, K., Monden, G., Miyazaki, N., Orn, C., Tsujimura, Y., Yoshida, S., Ma, J.F., and Ishii, T. (2017). Detection of quantitative trait loci controlling grain zinc concentration using Australian wild rice, Oryza meridionalis, a potential genetic resource for biofortification of rice. PLoS ONE 12: e0187224.
Ishimaru, Y., Masuda, H., Bashir, K., Inoue, H., Tsukamoto, T., Takahashi, M., Nakanishi, H., Aoki, N., Hirose, T., Ohsugi, R., and Nishizawa, N.K. (2010). Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J. 62: 379-390.
Ishimaru, Y., Suzuki, M., Tsukamoto, T., Suzuki, K., Nakazono, M., Kobayashi, T., Wada, Y., Watanabe, S., Matsuhashi, S., Takahashi, M., Nakanishi, H., Mori, S., and Nishizawa, N.K. (2006). Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J. 45: 335-346.
Johnson, A.A., Kyriacou, B., Callahan, D.L., Carruthers, L., Stangoulis, J., Lombi, E., and 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.
Kiely, M.E., McCarthy, E.K., and Hennessy, A. (2021). Iron, iodine and vitamin D deficiencies during pregnancy: Epidemiology, risk factors and developmental impacts. Proc. Nutr. Soc. 80: 290-302.
Kobayashi, T., Itai, R.N., Aung, M.S., Senoura, T., Nakanishi, H., and Nishizawa, N.K. (2012). The rice transcription factor IDEF1 directly binds to iron and other divalent metals for sensing cellular iron status. Plant J. 69: 81-91.
Kobayashi, T., Itai, R.N., Ogo, Y., Kakei, Y., Nakanishi, H., Takahashi, M., and Nishizawa, N.K. (2009). 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. 60: 948-961.
Kobayashi, T., Nagano, A.J., and Nishizawa, N.K. (2021). Iron deficiency-inducible peptide-coding genes OsIMA1 and OsIMA2 positively regulate a major pathway of iron uptake and translocation in rice. J. Exp. Bot. 72: 2196-2211.
Kobayashi, T., Nagasaka, S., Senoura, T., Itai, R.N., Nakanishi, H., and Nishizawa, N.K. (2013). Iron-binding haemerythrin RING ubiquitin ligases regulate plant iron responses and accumulation. Nat. Commun. 4: 2792.
Kobayashi, T., Ogo, Y., Itai, R.N., Nakanishi, H., Takahashi, M., Mori, S., and Nishizawa, N.K. (2007). The transcription factor IDEF1 regulates the response to and tolerance of iron deficiency in plants. Proc. Natl. Acad. Sci. U.S.A. 104: 19150-19155.
Koike, S., Inoue, H., Mizuno, D., Takahashi, M., Nakanishi, H., Mori, S., and Nishizawa, N.K. (2004). OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J. 39: 415-424.
Krishnappa, G., Singh, A.M., Chaudhary, S., Ahlawat, A.K., Singh, S.K., Shukla, R.B., Jaiswal, J.P., Singh, G.P., and Solanki, I.S. (2017). Molecular mapping of the grain iron and zinc concentration, protein content and thousand kernel weight in wheat (Triticum aestivum L.). PLoS ONE 12: e0174972.
Lee, S., and An, G. (2009). Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant Cell Environ. 32: 408-416.
Lee, S., Chiecko, J.C., Kim, S.A., Walker, E.L., Lee, Y., Guerinot, M.L., and An, G. (2009a). Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol. 150: 786-800.
Lee, S., Jeon, U.S., Lee, S.J., Kim, Y.-K., Persson, D.P., Husted, S., Schjørring, J.K., Kakei, Y., Masuda, H., Nishizawa, N.K., An, G. (2009b). Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proc. Natl. Acad. Sci. U.S.A. 106: 22014-22019.
Lee, S., Jeong, H.J., Kim, S.A., Lee, J., Guerinot, M.L., and An, G. (2010a). OsZIP5 is a plasma membrane zinc transporter in rice. Plant Mol. Biol. 73: 507-517.
Lee, S., Kim, S.A., Lee, J., Guerinot, M.L., and An, G. (2010b). Zinc deficiency-inducible OsZIP8 encodes a plasma membrane-localized zinc transporter in rice. Mol. Cells 29: 551-558.
Lee, S., Persson, D.P., Hansen, T.H., Husted, S., Schjoerring, J.K., Kim, Y.S., Jeon, U.S., Kim, Y.K., Kakei, Y., Masuda, H., Nishizawa, N.K., and An, G. (2011). Bio-available zinc in rice seeds is increased by activation tagging of nicotianamine synthase. Plant Biotechnol. J. 9: 865-873.
Li, D.Q., Wu, X.B., Wang, H.F., Feng, X., Yan, S.J., Wu, S.Y., Liu, J.X., Yao, X.F., Bai, A.N., Zhao, H., Song, X.F., Guo, L., Zhang, S.Y., and Liu, C.M. (2021). Defective mitochondrial function by mutation in THICK ALEURONE 1 encoding a mitochondrion-targeted single-stranded DNA binding protein leads to increased aleurone cell layers and improved nutrition in rice. Mol. Plant 14: 1343-1361.
Liang, G., Zhang, H., Li, Y., Pu, M., Yang, Y., Li, C., Lu, C., Xu, P., and Yu, D. (2020). Oryza sativa FER-LIKE FE DEFICIENCY-INDUCED TRANSCRIPTION FACTOR (OsFIT/OsbHLH156) interacts with OsIRO2 to regulate iron homeostasis. J. Integr. Plant Biol 62: 668-689.
Liu, D., Liu, Y., Zhang, W., Chen, X., and Zou, C. (2017). Agronomic approach of zinc biofortification can increase zinc bioavailability in wheat flour and thereby reduce zinc deficiency in humans. Nutrients 9: 465.
Liu, J., Wu, B., Singh, R.P., and Velu, G. (2019). QTL mapping for micronutrients concentration and yield component traits in a hexaploid wheat mapping population. J. Cereal Sci. 88: 57-64.
Liu, J., Wu, X., Yao, X., Yu, R., Larkin, P.J., and Liu, C.M. (2018). Mutations in the DNA demethylase OsROS1 result in a thickened aleurone and improved nutritional value in rice grains. Proc. Natl. Acad. Sci. U.S.A. 115: 11327-11332.
Liu, Y., Chen, Y., Yang, Y., Zhang, Q., Fu, B., Cai, J., Guo, W., Shi, L., Wu, J., and Chen, Y. (2021a). A thorough screening based on QTLs controlling zinc and copper accumulation in the grain of different wheat genotypes. Environ. Sci. Pollut. Res. Int. 28: 15043-15054.
Liu, Y., Kong, D., Wu, H.L., and Ling, H.Q. (2021b). Iron in plant-pathogen interactions. J. Exp. Bot. 72: 2114-2124.
Masuda, H., Ishimaru, Y., Aung, M.S., Kobayashi, T., Kakei, Y., Takahashi, M., Higuchi, K., Nakanishi, H., and Nishizawa, N.K. (2012). Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition. Sci. Rep. 2: 543.
Masuda, H., Usuda, K., Kobayashi, T., Ishimaru, Y., Kakei, Y., Takahashi, M., Higuchi, K., Nakanishi, H., Mori, S., and Nishizawa, N.K. (2009). Overexpression of the barley nicotianamine synthase gene HvNAS1 increases iron and zinc concentrations in rice grains. Rice 2: 155-166.
Nozoye, T., Nagasaka, S., Kobayashi, T., Takahashi, M., Sato, Y., Sato, Y., Uozumi, N., Nakanishi, H., and Nishizawa, N.K. (2011). Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J. Biol. Chem. 286: 5446-5454.
Ogo, Y., Kobayashi, T., Nakanishi Itai, R., Nakanishi, H., Kakei, Y., Takahashi, M., Toki, S., Mori, S., and Nishizawa, N.K. (2008). 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. 283: 13407-13417.
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.
Pearce, S., Tabbita, F., Cantu, D., Buffalo, V., Avni, R., Vazquez-Gross, H., Zhao, R., Conley, C.J., Distelfeld, A., and Dubcovksy, J. (2014). Regulation of Zn and Fe transporters by the GPC1 gene during early wheat monocarpic senescence. BMC Plant Biol. 14: 368.
Pradhan, S.K., Pandit, E., Pawar, S., Naveenkumar, R., Barik, S.R., Mohanty, S.P., Nayak, D.K., Ghritlahre, S.K., Sanjiba Rao, D., Reddy, J.N., and Patnaik, S.S.C. (2020). Linkage disequilibrium mapping for grain Fe and Zn enhancing QTLs useful for nutrient dense rice breeding. BMC Plant Biol. 20: 57.
Pramitha, J.L., Rana, S., Aggarwal, P.R., Ravikesavan, R., Joel, A.J., and Muthamilarasan, M. (2021). Diverse role of phytic acid in plants and approaches to develop low-phytate grains to enhance bioavailability of micronutrients. Adv. Genet. 107: 89-120.
Pyo, E., Tsang, B.L., and Parker, M.E. (2022). Rice as a vehicle for micronutrient fortification: A systematic review of micronutrient retention, organoleptic properties, and consumer acceptability. Nutr. Rev. 80: 1062-1085.
Qiao, K., Wang, F., Liang, S., Wang, H., Hu, Z., and Chai, T. (2019). New biofortification tool: Wheat TaCNR5 enhances zinc and manganese tolerance and increases zinc and manganese accumulation in rice grains. J. Agric. Food Chem. 67: 9877-9884.
Qu le, 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.
Ramzani, P.M., Khalid, M., Naveed, M., Ahmad, R., and Shahid, M. (2016). Iron biofortification of wheat grains through integrated use of organic and chemical fertilizers in pH affected calcareous soil. Plant Physiol. Biochem. 104: 284-293.
Ryu, M.-S., and Aydemir, T.B. (2020). Chapter 23 - Zinc. In: Marriott, B.P., Birt, D.F., Stallings, V.A., Yates, A.A., eds, Present Knowledge in Nutrition (Eleventh Edition), Academic Press, USA. pp. 393-408.
Sasaki, A., Yamaji, N., Mitani-Ueno, N., Kashino, M., and Ma, J.F. (2015). A node-localized transporter OsZIP3 is responsible for the preferential distribution of Zn to developing tissues in rice. Plant J. 84: 374-384.
Satoh-Nagasawa, N., Mori, M., Nakazawa, N., Kawamoto, T., Nagato, Y., Sakurai, K., Takahashi, H., Watanabe, A., and Akagi, H. (2012). Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol. 53: 213-224.
Satyavathi, C.T., Ambawat, S., Khandelwal, V., and Srivastava, R.K. (2021). Pearl millet: A climate-resilient nutricereal for mitigating hidden hunger and provide nutritional security. Front. Plant Sci. 12: 659938.
Semba, R.D., Askari, S., Gibson, S., Bloem, M.W., and Kraemer, K. (2022). The potential impact of climate change on the micronutrient-rich food supply. Adv. Nutr. 13: 80-100.
Senoura, T., Sakashita, E., Kobayashi, T., Takahashi, M., Aung, M.S., Masuda, H., Nakanishi, H., and Nishizawa, N.K. (2017). The iron-chelate transporter OsYSL9 plays a role in iron distribution in developing rice grains. Plant Mol. Biol. 95: 375-387.
Srinivasa, J., Arun, B., Mishra, V.K., Singh, G.P., Velu, G., Babu, R., Vasistha, N.K., and Joshi, A.K. (2014). Zinc and iron concentration QTL mapped in a Triticum spelta x T. aestivum cross. Theor. Appl. Genet. 127: 1643-1651.
Suman, K., Neeraja, C.N., Madhubabu, P., Rathod, S., Bej, S., Jadhav, K.P., Kumar, J.A., Chaitanya, U., Pawar, S.C., Rani, S.H., Subbarao, L.V., and Voleti, S.R. (2021). Identification of promising RILs for high grain zinc through genotype x environment analysis and stable grain zinc QTL using SSRs and SNPs in rice (Oryza sativa L.). Front. Plant Sci. 12: 587482.
Sun, H., Du, W., Peng, Q., Lv, Z., Mao, H., and Kopittke, P.M. (2020). Development of ZnO nanoparticles as an efficient Zn fertilizer: Using synchrotron-based techniques and laser ablation to examine elemental distribution in wheat grain. J. Agric. Food Chem. 68: 5068-5075.
Swamy, B.P.M., Marathi, B., Ribeiro-Barros, A.I.F., Calayugan, M.I.C., and Ricachenevsky, F.K. (2021). Iron biofortification in rice: An update on quantitative trait loci and candidate genes. Front. Plant Sci. 12: 647341.
Takahashi, R., Ishimaru, Y., Shimo, H., Ogo, Y., Senoura, T., Nishizawa, N.K., and 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.
Takahashi, M., Yamaguchi, H., Nakanishi, H., Shioiri, T., Nishizawa, N.-K., and 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.
Tan, J., Wang, J., Chai, T., Zhang, Y., Feng, S., Li, Y., Zhao, H., Liu, H., and Chai, X. (2013). Functional analyses of TaHMA2, a P(1B)-type ATPase in wheat. Plant Biotechnol. J. 11: 420-431.
Tan, L., Qu, M., Zhu, Y., Peng, C., Wang, J., Gao, D., and Chen, C. (2020). ZINC TRANSPORTER5 and ZINC TRANSPORTER9 function synergistically in zinc/cadmium uptake. Plant Physiol. 183: 1235-1249.
Tanaka, K., Yoshida, T., Asada, K., and Kasai, Z. (1973). Subcellular particles isolated from aleurone layer of rice seeds. Arch. Biochem. Biophys. 155: 136-143.
Trijatmiko, K.R., Duenas, C., Tsakirpaloglou, N., Torrizo, L., Arines, F.M., Adeva, C., Balindong, J., Oliva, N., Sapasap, M.V., Borrero, J., Rey, J., Francisco, P., Nelson, A., Nakanishi, H., Lombi, E., Tako, E., Glahn, R.P., Stangoulis, J., Chadha-Mohanty, P., Johnson, A.A.T., Tohme, J., Barry, G., and Slamet-Loedin, I.H. (2016). Biofortified indica rice attains iron and zinc nutrition dietary targets in the field. Sci. Rep. 6: 19792.
Uauy, C., Distelfeld, A., Fahima, T., Blechl, A., and Dubcovsky, J. (2006). A NAC Gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314: 1298-1301.
Vasconcelos, M., Datta, K., Oliva, N., Khalekuzzaman, M., Torrizo, L., Krishnan, S., Oliveira, M., Goto, F., and Datta, S.K. (2003). Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. Plant Sci. 164: 371-378.
Velu, G., Singh, R.P., Crespo-Herrera, L., Juliana, P., Dreisigacker, S., Valluru, R., Stangoulis, J., Sohu, V.S., Mavi, G.S., Mishra, V.K., Balasubramaniam, A., Chatrath, R., Gupta, V., Singh, G.P., and Joshi, A.K. (2018). Genetic dissection of grain zinc concentration in spring wheat for mainstreaming biofortification in CIMMYT wheat breeding. Sci. Rep. 8: 13526.
Velu, G., Tutus, Y., Gomez-Becerra, H.F., Hao, Y., Demir, L., Kara, R., Crespo-Herrera, L.A., Orhan, S., Yazici, A., Singh, R.P., and Cakmak, I. (2016). QTL mapping for grain zinc and iron concentrations and zinc efficiency in a tetraploid and hexaploid wheat mapping populations. Plant Soil 411: 81-99.
Wang, H., Liao, S., Li, M., Wei, J., Zhu, B., Gu, L., Li, L., and Du, X. (2022). TmNAS3 from Triticum monococum directly regulated by TmbHLH47 increases Fe content of wheat grain. Gene 811: 146096.
Wang, S., Li, L., Ying, Y., Wang, J., Shao, J.F., Yamaji, N., Whelan, J., Ma, J.F., and Shou, H. (2020). A transcription factor OsbHLH156 regulates Strategy II iron acquisition through localising IRO2 to the nucleus in rice. New Phytol. 225: 1247-1260.
Wang, Y., Meng, Y., Ma, Y., Liu, L., Wu, D., Shu, X., Pan, L., and Lai, Q. (2021). Combination of high Zn density and low phytic acid for improving Zn bioavailability in rice (Oryza stavia L.) grain. Rice (N Y) 14: 23.
Waters, B.M., Uauy, C., Dubcovsky, J., and Grusak, M.A. (2009). Wheat (Triticum aestivum) NAM proteins regulate the translocation of iron, zinc, and nitrogen compounds from vegetative tissues to grain. J. Exp. Bot. 60: 4263-4274.
Wei, Y., Shohag, M.J., and Yang, X. (2012). Biofortification and bioavailability of rice grain zinc as affected by different forms of foliar zinc fertilization. PLoS ONE 7: e45428.
Williams, S.G. (1970). The role of phytic acid in the wheat grain. Plant Physiol. 45: 376-381.
Wirth, J., Poletti, S., Aeschlimann, B., Yakandawala, N., Drosse, B., Osorio, S., Tohge, T., Fernie, A.R., Gunther, D., Gruissem, W., and Sautter, C. (2009). Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin. Plant Biotechnol. J. 7: 631-644.
Yamaji, N., Xia, J., Mitani-Ueno, N., Yokosho, K., and Feng Ma, J. (2013). Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiol. 162: 927-939.
Yang, M., Li, Y., Liu, Z., Tian, J., Liang, L., Qiu, Y., Wang, G., Du, Q., Cheng, D., Cai, H., Shi, L., Xu, F., and Lian, X. (2020). A high activity zinc transporter OsZIP9 mediates zinc uptake in rice. Plant J. 103: 1695-1709.
Yokosho, K., Yamaji, N., and Ma, J.F. (2016). OsFRDL1 expressed in nodes is required for distribution of iron to grains in rice. J. Exp. Bot. 67: 5485-5494.
Yokosho, K., Yamaji, N., Ueno, D., Mitani, N., and Ma, J.F. (2009). OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol. 149: 297-305.
Zhang, G.M., Zheng, T.Q., Chen, Z., Wang, Y.L., Wang, Y., Shi, Y.M., Wang, C.C., Zhang, L.Y., Ma, J.T., Deng, L.W., Li, W., Xu, T.T., Liang, C.Z., Xu, J.L., and Li, Z.K. (2018a). Joint exploration of favorable haplotypes for mineral concentrations in milled grains of rice (Oryza sativa L.). Front. Plant Sci. 9: 447.
Zhang, H., Li, Y., Pu, M., Xu, P., Liang, G., and Yu, D. (2020). Oryza sativa POSITIVE REGULATOR OF IRON DEFICIENCY RESPONSE 2 (OsPRI2) and OsPRI3 are involved in the maintenance of Fe homeostasis. Plant Cell Environ. 43: 261-274.
Zhang, H., Li, Y., Yao, X., Liang, G., and Yu, D. (2017). POSITIVE REGULATOR OF IRON HOMEOSTASIS1, OsPRI1, facilitates iron homeostasis. Plant Physiol. 175: 543-554.
Zhang, T., Sun, H., Lv, Z., Cui, L., Mao, H., and Kopittke, P.M. (2018b). Using synchrotron-based approaches to examine the foliar application of ZnSO4 and ZnO aanoparticles for field-grown winter wheat. J. Agric. Food Chem. 66: 2572-2579.
Zhang, Y., Shi, R., Rezaul, K.M., Zhang, F., and Zou, C. (2010). Iron and zinc concentrations in grain and flour of winter wheat as affected by foliar application. J. Agric. Food Chem. 58: 12268-12274.
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. Plant J. 72: 400-410.
Zheng, L., Cheng, Z., Ai, C., Jiang, X., Bei, X., Zheng, Y., Glahn, R.P., Welch, R.M., Miller, D.D., Lei, X.G., and Shou, H. (2010). Nicotianamine, a novel enhancer of rice iron bioavailability to humans. PLoS ONE 5: e10190.