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Micronutrient Movement and Signalling in Plants from a Biofortification Perspective

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Plant Micronutrients

Abstract

Micronutrients are crucial for plant development and play a significant role in balanced crop nutrition. The micronutrients, viz. zinc (Zn), iron (Fe), copper (Cu) and manganese (Mn), are essential for plants and humans that are directly or indirectly dependent on plants. These essential mineral elements regulate crucial cellular processes, viz. respiration (Fe and Cu), photosynthesis (Fe, Cu and Mn), and transcription (Zn). The uptake, distribution and storage of micronutrients under physiological conditions should be tightly regulated to guarantee optimum metabolic rates and to evade excessive toxic levels. Variation in the equilibrium of uptake, transport or storage of these nutrients can severely impair cellular metabolism and distress plant development and growth. The micronutrient uptake from the environment, its distribution to several organs and tissues, and subcellular compartmentalisation require the metal to cross various membranes. The intracellular compartments are linked through intricate retrograde signalling cascades to regulate cellular metal homeostasis. Plants have developed complex functional mechanisms to acclimate with variable micronutrient accessibility. These processes are under the regulation of long- and short-distance signalling pathways. Several molecular components involved in micronutrient acquisition in the local and long-range regulatory routes in addition to their putative sites in the signalling cascade have been recognised. All these transport events are strictly regulated at transcriptional and post-translational stages. This short- and long-range incitation works at the fundamental and functional levels to synchronise nutrient homeostasis at the local and systemic levels. A few entities belonging to several gene families are hypothesised to perform key roles in micronutrient dispersal throughout the plant. The integration of these transduction signals acts at the cellular and entire plant levels to maintain nutrient homeostasis at the local and systemic scales.

Biofortification or an increase in the micronutrient density of chief crops will significantly improve human sustenance on a global level. Several annotations point to an unexpected interconnection in the homeostasis of different micronutrients. In spite of their vital status and biotic significance, these interactions remain principally unidentified. Thus, this chapter aims at addressing some of the most topical advances in micronutrient movement from soil to seed as well as cellular and subcellular homeostasis mechanisms in plants. Here, recent knowledge on the regulation of the transporters, proteins, genes and signalling of Fe, Mn, Zn and Cu individually is discussed. This will delineate a novel platform to provide an overview of potential strategies that can be used to regulate metabolism, increase flexibility to diverse environmental conditions, improve nutritional status and generate biofortified crop plants in the future.

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References

  • Afzal, S., Sirohi, P., Yadav, A. K., Singh, M. P., Kumar, A., & Singh, N. K. (2019). A comparative screening of abiotic stress tolerance in early flowering rice mutants. Journal of Biotechnology, 302, 112–122.

    Article  CAS  PubMed  Google Scholar 

  • Aguirre, G., & Pilon, M. (2016). Copper delivery to chloroplast proteins and its regulation. Frontiers in Plant Science, 6, 1250.

    Article  PubMed  PubMed Central  Google Scholar 

  • Alagić, S. Č., Tošić, S. B., Dimitrijević, M. D., Nujkić, M. M., Papludis, A. D., & Fogl, V. Z. (2018). The content of the potentially toxic elements, iron and manganese, in the grapevine cv Tamjanika growing near the biggest copper mining/metallurgical complex on the Balkan peninsula: Phytoremediation, biomonitoring, and some toxicological aspects. Environmental Science and Pollution Research, 25(34), 34139–34154.

    Article  PubMed  CAS  Google Scholar 

  • Aller, S. G., & Unger, V. M. (2006). Projection structure of the human copper transporter CTR1 at 6-Å resolution reveals a compact trimer with a novel channel-like architecture. Proceedings of the National Academy of Sciences, 103(10), 3627–3632.

    Article  CAS  Google Scholar 

  • Alloway, B. J. (2009). Soil factors associated with zinc deficiency in crops and humans. Environmental Geochemistry and Health, 31, 537–548.

    Article  CAS  PubMed  Google Scholar 

  • Anaemias, W. N. (2017). Tools for effective prevention and control. Geneva: World Health Organisation.

    Google Scholar 

  • Andrés-Colás, N., Sancenón, V., Rodríguez-Navarro, S., Mayo, S., Thiele, D. J., Ecker, J. R., Puig, S., & Peñarrubia, L. (2006). The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. The Plant Journal, 45(2), 225–236.

    Article  PubMed  CAS  Google Scholar 

  • Arnold, T. I. M., Kirk, G. J., Wissuwa, M., Frei, M., Zhao, F. J., Mason, T. F., & Weiss, D. J. (2010). Evidence for the mechanisms of zinc uptake by rice using isotope fractionation. Plant, Cell & Environment, 33(3), 370–381.

    Article  CAS  Google Scholar 

  • Banakar, R., Alvarez Fernandez, A., Díaz-Benito, P., Abadia, J., Capell, T., & Christou, P. (2017). Phytosiderophores determine thresholds for iron and zinc accumulation in biofortified rice endosperm while inhibiting the accumulation of cadmium. Journal of Experimental Botany, 68(17), 4983–4995.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barberon, M., Zelazny, E., Robert, S., Conéjéro, G., Curie, C., Friml, J., & Vert, G. (2011). Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proceedings of the National Academy of Sciences, 108(32), E450–E458.

    Article  CAS  Google Scholar 

  • Bashir, K., Inoue, H., Nagasaka, S., Takahashi, M., Nakanishi, H., Mori, S., et al. (2006). Cloning and characterization of deoxymugineic acid synthase genes from graminaceous plants. Journal of Biological Chemistry, 281, 32395–32402. https://doi.org/10.1074/jbc.m604133200.

    Article  CAS  Google Scholar 

  • Bashir, K., Ishimaru, Y., Itai, R. N., Senoura, T., Takahashi, M., An, G., Oikawa, T., Ueda, M., Sato, A., Uozumi, N., Nakanishi, H., & Nishizawa, N. K. (2015). Iron deficiency regulated OsOPT7 is essential for iron homeostasis in rice. Plant Molecular Biology, 88, 165–176. https://doi.org/10.1007/s11103-015-0315-0.

    Article  CAS  PubMed  Google Scholar 

  • Bashir, K., Nozoye, T., Nagasaka, S., Rasheed, S., Miyauchi, N., Seki, M., Nakanishi, H., & Nishizawa, N. K. (2017). Paralogs and mutants show that one DMA synthase functions in iron homeostasis in rice. Journal of Experimental Botany, 68(7), 1785–1795.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bashir, K., Rasheed, S., Kobayashi, T., Seki, M., & Nishizawa, N. K. (2016). Regulating subcellular metal homeostasis: The key to crop improvement. Frontiers in Plant Science, 7, 1192.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bashir, K., Takahashi, R., Akhtar, S., Ishimaru, Y., Nakanishi, H., & Nishizawa, N. K. (2013). The knockdown of OsVIT2 and MIT affects iron localization in rice seed. Rice, 6(1), 31.

    Article  PubMed  PubMed Central  Google Scholar 

  • Benatti, M. R., Yookongkaew, N., Meetam, M., Guo, W.-J., Punyasuk, N., AbuQamar, S., et al. (2014). Metallothionein deficiency impacts copper accumulation and redistribution in leaves and seeds of Arabidopsis. New Phytologist, 202, 940–951. https://doi.org/10.1111/nph.12718.

    Article  CAS  Google Scholar 

  • Blaby-Haas, C. E., Padilla-Benavides, T., Stübe, R., Argüello, J. M., & Merchant, S. S. (2014). Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis. Proceedings of the National Academy of Sciences, 111(50), E5480–E5487.

    Article  CAS  Google Scholar 

  • Blindauer, C. A., & Schmid, R. (2010). Cytosolic metal handling in plants: Determinants for zinc specificity in metal transporters and metallothioneins. Metallomics, 2(8), 510–529.

    Article  CAS  PubMed  Google Scholar 

  • Boonyaves, K., Gruissem, W., & Bhullar, N. K. (2016). NOD promoter-controlled AtIRT1 expression functions synergistically with NAS and FERRITIN genes to increase iron in rice grains. Plant Molecular Biology, 90(3), 207–215.

    Article  CAS  PubMed  Google Scholar 

  • Bowler, C., Slooten, L., Vandenbranden, S., De Rycke, R., Botterman, J., Sybesma, C., Van Montagu, M., & Inzé, D. (1991). Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. The EMBO Journal, 10(7), 1723–1732.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bozzi, A. T., Zimanyi, C. M., Nicoludis, J. M., Lee, B. K., Zhang, C. H., & Gaudet, R. (2019). Structures in multiple conformations reveal distinct transition metal and proton pathways in an Nramp transporter. eLife, 8, e41124.

    Article  PubMed  PubMed Central  Google Scholar 

  • Broadley, M., Brown, P., Cakmak, I., Rengel, Z., & Zhao, F. (2011). Function of nutrients: Micronutrients. In Marschner’s mineral nutrition of higher plants (pp. 191–248). London: Academic Press.

    Google Scholar 

  • Broadley, M., Brown, P., Cakmak, I., Rengel, Z., & Zhao, F. (2012). Function of nutrients: Micronutrients. In Marschner’s mineral nutrition of higher plants (pp. 191–248). London: Academic Press.

    Chapter  Google Scholar 

  • Cailliatte, R., Schikora, A., Briat, J. F., Mari, S., & Curie, C. (2010). High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. The Plant Cell, 22(3), 904–917.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cakmak, I., Kalayci, M., Kaya, Y., Torun, A. A., Aydin, N., Wang, Y., Arisoy, Z., Erdem, H., Yazici, A., Gokmen, O., & Ozturk, L. (2010). Biofortification and localization of zinc in wheat grain. Journal of Agricultural and Food Chemistry, 58(16), 9092–9102.

    Article  CAS  PubMed  Google Scholar 

  • Cellier, M., Belouchi, A., & Gros, P. (1996). Resistance to intracellular infections: Comparative genomic analysis of Nramp. Trends in Genetics, 12(6), 201–204.

    Article  CAS  PubMed  Google Scholar 

  • Cellier, M., Prive, G., Belouchi, A., Kwan, T., Rodrigues, V., Chia, W., & Gros, P. (1995). Nramp defines a family of membrane proteins. Proceedings of the National Academy of Sciences, 92(22), 10089–10093.

    Article  CAS  Google Scholar 

  • Che, J., Yamaji, N., & Ma, J. F. (2018). Efficient and flexible uptake system for mineral elements in plants. New Phytologist, 219(2), 513–517.

    Article  CAS  Google Scholar 

  • Chen, X., Li, J., Wang, L., Ma, G., & Zhang, W. (2016). A mutagenic study identifying critical residues for the structure and function of rice manganese transporter OsMTP8.1. Scientific Reports, 6(1), 1–11.

    Article  CAS  Google Scholar 

  • Chen, Z., Fujii, Y., Yamaji, N., Masuda, S., Takemoto, Y., Kamiya, T., Yusuyin, Y., Iwasaki, K., Kato, S. I., Maeshima, M., & Ma, J. F. (2013). Mn tolerance in rice is mediated by MTP8. 1, a member of the cation diffusion facilitator family. Journal of Experimental Botany, 64(14), 4375–4387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng, L., Wang, F., Shou, H., Huang, F., Zheng, L., He, F., Li, J., Zhao, F. J., Ueno, D., Ma, J. F., & Wu, P. (2007). Mutation in nicotianamine aminotransferase stimulated the Fe (II) acquisition system and led to iron accumulation in rice. Plant Physiology, 145(4), 1647–1657.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarkson, D. T. (1988). The uptake and translocation of manganese by plant roots. In Manganese in soils and plants (pp. 101–111). Dordrecht: Springer.

    Chapter  Google Scholar 

  • Connorton, J. M., Jones, E. R., Rodríguez-Ramiro, I., Fairweather-Tait, S., Uauy, C., & Balk, J. (2017). Wheat vacuolar iron transporter TaVIT2 transports Fe and Mn and is effective for biofortification. Plant Physiology, 174(4), 2434–2444.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conte, S. S., Chu, H. H., Rodriguez, D. C., Punshon, T., Vasques, K. A., Salt, D. E., et al. (2013). Arabidopsis thaliana Yellow stripe1-Like4 and Yellow Stripe1-Like6 localize to internal cellular membranes and are involved in metal ion homeostasis. Frontiers in Plant Science, 4, 283. https://doi.org/10.3389/fpls.2013.00283.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Curie, C., Cassin, G., Couch, D., Divol, F., Higuchi, K., Le Jean, M., Misson, J., Schikora, A., Czernic, P., & Mari, S. (2009). Metal movement within the plant: Contribution of nicotianamine and yellow stripe 1-like transporters. Annals of Botany, 103(1), 1–11.

    Article  CAS  PubMed  Google Scholar 

  • Curie, C., Panaviene, Z., Loulergue, C., Dellaporta, S. L., Briat, J. F., & Walker, E. L. (2001). Maize yellow stripe1 encodes a membrane protein directly involved in Fe (III) uptake. Nature, 409(6818), 346.

    Article  CAS  PubMed  Google Scholar 

  • del Pozo, T., Cambiazo, V., & González, M. (2010). Gene expression profiling analysis of copper homeostasis in Arabidopsis thaliana. Biochemical and Biophysical Research Communications, 393(2), 248–252.

    Article  PubMed  CAS  Google Scholar 

  • Delhaize, E., Gruber, B. D., Pittman, J. K., White, R. G., Leung, H., Miao, Y., Jiang, L., Ryan, P. R., & Richardson, A. E. (2007). A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. The Plant Journal, 51(2), 198–210.

    Article  CAS  PubMed  Google Scholar 

  • Delhaize, E., Kataoka, T., Hebb, D. M., White, R. G., & Ryan, P. R. (2003). Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. The Plant Cell, 15(5), 1131–1142.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Demidchik, V., & Maathuis, F. J. (2007). Physiological roles of nonselective cation channels in plants: From salt stress to signalling and development. New Phytologist, 175(3), 387–404.

    Article  CAS  Google Scholar 

  • Deng, F., Yamaji, N., Xia, J., & Ma, J. F. (2013). A member of the heavy metal P-type ATPase OsHMA5 is involved in xylem loading of copper in rice. Plant Physiology, 163(3), 1353–1362.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhoke, S. K., Mahajan, P., Kamble, R., & Khanna, A. (2013). Effect of nanoparticles suspension on the growth of mung (Vigna radiata) seedlings by foliar spray method. Nanotechnology Development, 3(1), e1–e1.

    Article  CAS  Google Scholar 

  • DiDonato, R. J., Jr., Roberts, L. A., Sanderson, T., Eisley, R. B., & Walker, E. L. (2004). Arabidopsis Yellow Stripe-Like2 (YSL2): A metal-regulated gene encoding a plasma membrane transporter of nicotianamine–metal complexes. The Plant Journal, 39(3), 403–414.

    Article  CAS  PubMed  Google Scholar 

  • Doberman, A., & Fairhurst, T. (2000). Rice: Nutrient disorders and nutrient management. Makati City & Singapore: IRRI & PPI & PPIC.

    Google Scholar 

  • Dong, B., Rengel, Z., & Graham, R. D. (1995). Root morphology of wheat genotypes differing in zinc efficiency. Journal of Plant Nutrition, 18(12), 2761–2773.

    Article  CAS  Google Scholar 

  • Donner, E., Punshon, T., Guerinot, M. L., et al. (2012). Analytical and Bioanalytical Chemistry, 402, 3287. https://doi.org/10.1007/s00216-011-5624-9.

    Article  CAS  PubMed  Google Scholar 

  • Durrett, T. P., Gassmann, W., & Rogers, E. E. (2007). The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiology, 144(1), 197–205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eaton, T. E. (2015). Manganese. In A. V. Barker & D. J. Pilbeam (Eds.), Handbook of plant nutrition (pp. 427–485). Boca Raton: CRC Press.

    Chapter  Google Scholar 

  • Erenoglu, E. B., Kutman, U. B., Ceylan, Y., Yildiz, B., & Cakmak, I. (2011). Improved nitrogen nutrition enhances root uptake, root-to-shoot translocation and remobilization of zinc (65Zn) in wheat. New Phytology, 189, 438–448. https://doi.org/10.1111/j.1469-8137.2010.03488.x.

    Article  CAS  Google Scholar 

  • Eroglu, S., et al. (2016). The vacuolar manganese transporter MTP8 determines tolerance to iron deficiency-induced chlorosis in Arabidopsis. Plant Physiology, 170, 1030–1045.

    Article  CAS  PubMed  Google Scholar 

  • Fernando, D. R., Bakkaus, E. J., Perrier, N., Baker, A. J., Woodrow, I. E., Batianoff, G. N., et al. (2006a). Manganese accumulation in the leaf mesophyll of four tree species: A PIXE/EDAX localization study. New Phytology, 171, 751–757. https://doi.org/10.1111/j.1469-8137.2006.01783.x.

    Article  CAS  Google Scholar 

  • Fernando, D. R., Batianoff, G. N., Baker, A. J., & Woodrow, I. E. (2006b). In vivo localization of manganese in the hyperaccumulator Gossia bidwillii (Benth.) N. Snow & Guymer (Myrtaceae) by cryo-SEM/EDAX. Plant Cell Environment, 29, 1012–1020. https://doi.org/10.1111/j.1365-3040.2006.01498.x.

    Article  CAS  Google Scholar 

  • Fernando, D. R., & Lynch, J. P. (2015). Manganese phytotoxicity: New light on an old problem. Annals of Botany, 116, 313–319.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernando, D. R., et al. (2009). Foliar Mn accumulation in eastern Australian herbarium specimens: Prospecting for ‘new’ Mn hyperaccumulators and potential applications in taxonomy. Annals of Botany, 104, 357–357.

    Article  CAS  PubMed Central  Google Scholar 

  • Frei, M., Wang, Y., Ismail, A. M., & Wissuwa, M. (2010). Biochemical factors conferring shoot tolerance to oxidative stress in rice grown in low zinc soil. Functional Plant Biology, 37(1), 74–84.

    Article  CAS  Google Scholar 

  • Garcia-Molina, A., Andrés-Colás, N., Perea-García, A., Neumann, U., Dodani, S. C., Huijser, P., Peñarrubia, L., & Puig, S. (2013). The Arabidopsis COPT6 transport protein functions in copper distribution under copper-deficient conditions. Plant and Cell Physiology, 54(8), 1378–1390.

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez, A., Koren’Kov, V., & Wagner, G. J. (1999). A comparison of Zn, Mn, Cd, and Ca transport mechanisms in oat root tonoplast vesicles. Physiologia Plantarum, 106(2), 203–209.

    Article  CAS  Google Scholar 

  • Goto, F., Yoshihara, T., Shigemoto, N., Toki, S., & Takaiwa, F. (1999). Iron fortification of rice seed by the soybean ferritin gene. Nature Biotechnology, 17(3), 282.

    Article  CAS  PubMed  Google Scholar 

  • Gross, J., Stein, R. J., Fett-Neto, A. G., & Fett, J. P. (2003). Iron homeostasis related genes in rice. Genetics and Molecular Biology, 26(4), 477–497.

    Article  CAS  Google Scholar 

  • Grotz, N., Fox, T., Connolly, E., Park, W., Guerinot, M. L., & Eide, D. (1998). Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proceedings of the National Academy of Sciences, 95(12), 7220–7224.

    Article  CAS  Google Scholar 

  • Guo, W.-J., Bundithya, W., & Goldsbrough, P. B. (2003). Characterization of the Arabidopsis metallothione in gene family: Tissue-specific expression and induction during senescence and in response to copper. New Phytologist, 159, 369–381. https://doi.org/10.1046/j.1469-8137.2003.00813.x.

    Article  CAS  Google Scholar 

  • Hanikenne, M., Talke, I. N., Haydon, M. J., Lanz, C., Nolte, A., Motte, P., Kroymann, J., Weigel, D., & Krämer, U. (2008). Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature, 453(7193), 391.

    Article  CAS  PubMed  Google Scholar 

  • Haydon, M. J., & Cobbett, C. S. (2007). Transporters of ligands for essential metal ions in plants. New Phytologist, 174(3), 499–506.

    Article  CAS  Google Scholar 

  • He, J., Zhang, R. X., Peng, K., Tagliavia, C., Li, S., Xue, S., Liu, A., Hu, H., Zhang, J., Hubbard, K. E., Held, K., McAinsh, M. R., Gray, J. E., Kudla, J., Schroeder, J. I., Liang, Y. K., & Hetherington, A. M. (2018). The BIG protein distinguishes the process of CO2-induced stomatal closure from the inhibition of stomatal opening by CO2. New Phytology, 218, 232–241.

    Article  CAS  Google Scholar 

  • Henriques, R., Jásik, J., Klein, M., Martinoia, E., Feller, U., Schell, J., Pais, M. S., & Koncz, C. (2002). Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Molecular Biology, 50(4-5), 587–597.

    Article  CAS  PubMed  Google Scholar 

  • Hernández, L. E., Lozano-Rodrıguez, E., Gárate, A., & Carpena-Ruiz, R. (1998). Influence of cadmium on the uptake, tissue accumulation and subcellular distribution of manganese in pea seedlings. Plant Science, 132(2), 139–151.

    Article  Google Scholar 

  • Hotz, C., & Brown, K. H. (2004. International Zinc Nutrition Consultative Group (IZiNCG)). Technical document #1. Assessment of the risk of zinc deficiency in populations and options for its control. Food and Nutrition Bulletin, 25, S91–S203.

    Google Scholar 

  • Huffman, D. L., & O’Halloran, T. V. (2001). Function, structure, and mechanism of intracellular copper trafficking proteins. Annual Review of Biochemistry, 70(1), 677–701.

    Article  CAS  PubMed  Google Scholar 

  • Hussain, D., Haydon, M. J., Wang, Y., Wong, E., Sherson, S. M., Young, J., Camakaris, J., Harper, J. F., & Cobbett, C. S. (2004). P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. The Plant Cell, 16(5), 1327–1339.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Impa, S. M., & Johnson-Beebout, S. E. (2012). Mitigating zinc deficiency and achieving high grain Zn in rice through integration of soil chemistry and plant physiology research. Plant and Soil, 361(1-2), 3–41.

    Article  CAS  Google Scholar 

  • Inoue, H., Kobayashi, T., Nozoye, T., Takahashi, M., Kakei, Y., Suzuki, K., Nakazono, M., Nakanishi, H., Mori, S., & Nishizawa, N. K. (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. Journal of Biological Chemistry, 284(6), 3470–3479.

    Article  CAS  Google Scholar 

  • Inoue, H., Takahashi, M., Kobayashi, T., Suzuki, M., Nakanishi, H., Mori, S., & Nishizawa, N. K. (2008). Identification and localisation of the rice nicotianamine aminotransferase gene OsNAAT1 expression suggests the site of phytosiderophore synthesis in rice. Plant Molecular Biology, 66(1–2), 193–203.

    Article  CAS  PubMed  Google Scholar 

  • Ishimaru, Y., Masuda, H., Bashir, K., Inoue, H., Tsukamoto, T., Takahashi, M., Nakanishi, H., Aoki, N., Hirose, T., Ohsugi, R., & Nishizawa, N. K. (2010). Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. The Plant Journal, 62(3), 379–390.

    Article  CAS  PubMed  Google Scholar 

  • Ishimaru, Y., Suzuki, M., Kobayashi, T., Takahashi, M., Nakanishi, H., Mori, S., & Nishizawa, N. K. (2005). OsZIP4, a novel zinc-regulated zinc transporter in rice. Journal of Experimental Botany, 56(422), 3207–3214.

    Article  CAS  PubMed  Google Scholar 

  • Ishimaru, Y., Suzuki, M., Tsukamoto, T., Suzuki, K., Nakazono, M., Kobayashi, T., Wada, Y., Watanabe, S., Matsuhashi, S., Takahashi, M., & Nakanishi, H. (2006). Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. The Plant Journal, 45(3), 335–346.

    Article  CAS  PubMed  Google Scholar 

  • Jain, A., Wilson, G. T., & Connolly, E. L. (2014). The diverse roles of FRO family metalloreductases in iron and copper homeostasis. Frontiers in Plant Science, 5, 100.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jean, M. L., Schikora, A., Mari, S., Briat, J. F., & Curie, C. (2005). A loss-of-function mutation in AtYSL1 reveals its role in iron and nicotianamine seed loading. The Plant Journal, 44(5), 769–782.

    Article  PubMed  CAS  Google Scholar 

  • Jeong, J., & Connolly, E. L. (2009). Iron uptake mechanisms in plants: Functions of the FRO family of ferric reductases. Plant Science, 176(6), 709–714.

    Article  CAS  Google Scholar 

  • Jiang, Y. M., Mo, X. A., Du, F. Q., Fu, X., Zhu, X. Y., Gao, H. Y., Xie, J. L., Liao, F. L., Pira, E., & Zheng, W. (2006). Effective treatment of manganese-induced occupational Parkinsonism with p-aminosalicylic acid: A case of 17-year follow-up study. Journal of Occupational and Environmental Medicine/American College of Occupational and Environmental Medicine, 48(6), 644.

    Article  PubMed Central  Google Scholar 

  • Johnson, A. A., Kyriacou, B., Callahan, D. L., 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(9), e24476.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jonak, C., Nakagami, H., & Hirt, H. (2004). Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiology, 136(2), 3276–3283.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung, J. K. H. M., & McCouch, S. R. M. (2013). Getting to the roots of it: Genetic and hormonal control of root architecture. Frontiers in Plant Science, 4, 186.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kakei, Y., Ishimaru, Y., Kobayashi, T., Yamakawa, T., Nakanishi, H., & Nishizawa, N. K. (2012). OsYSL16 plays a role in the allocation of iron. Plant Molecular Biology, 79(6), 583–594.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamiya, T., Akahori, T., & Maeshima, M. (2005). Expression profile of the genes for rice cation/H+ exchanger family and functional analysis in yeast. Plant and Cell Physiology, 46(10), 1735–1740.

    Article  CAS  PubMed  Google Scholar 

  • Kamiya, T., & Maeshima, M. (2004). Residues in internal repeats of the rice cation/H+ exchanger are involved in the transport and selection of cations. Journal of Biological Chemistry, 279(1), 812–819.

    Article  CAS  Google Scholar 

  • Kawachi, M., Kobae, Y., Mori, H., Tomioka, R., Lee, Y., & Maeshima, M. (2009). A mutant strain Arabidopsis thaliana that lacks vacuolar membrane zinc transporter MTP1 revealed the latent tolerance to excessive zinc. Plant and Cell Physiology, 50(6), 1156–1170.

    Article  CAS  PubMed  Google Scholar 

  • Kim, S. A., & Guerinot, M. L. (2007). Mining iron: Iron uptake and transport in plants. FEBS Letters, 581(12), 2273–2280.

    Article  CAS  PubMed  Google Scholar 

  • Kitagishi, K., & Yamane, I. (1981). In K. Kitahishi & I. Yamane (Eds.), Heavy metal pollution in soils of Japan (pp. 1–302). Tokyo: Japan Science Society Press.

    Google Scholar 

  • Kobayashi, T., Itai, R. N., Ogo, Y., Kakei, Y., Nakanishi, H., Takahashi, M., & 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. The Plant Journal, 60(6), 948–961.

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi, T., & Nishizawa, N. K. (2012). Iron uptake, translocation, and regulation in higher plants. Annual Review of Plant Biology, 63, 131–152. https://doi.org/10.1146/annurev-arplant-042811-105522.

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi, T., Suzuki, M., Inoue, H., Itai, R. N., Takahashi, M., Nakanishi, H., & Nishizawa, N. K. (2005). Expression of iron-acquisition-related genes in iron-deficient rice is co-ordinately induced by partially conserved iron-deficiency-responsive elements. Journal of Experimental Botany, 56(415), 1305–1316.

    Google Scholar 

  • Koike, S., Inoue, H., Mizuno, D., Takahashi, M., Nakanishi, H., Mori, S., & Nishizawa, N. K. (2004). OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. The Plant Journal, 39(3), 415–424.

    Article  CAS  PubMed  Google Scholar 

  • Krishnan, S., & Dayanandan, P. (2003). Structural and histochemical studies on grain-filling in the caryopsis of rice (Oryza sativa L.). Journal of Biosciences, 28(4), 455–469.

    Article  CAS  PubMed  Google Scholar 

  • Lanaras, T., Moustakas, M., Symeonidis, L., Diamantoglou, S., & Karataglis, S. (1993). Plant metal content, growth responses and some photosynthetic measurements on field-cultivated wheat growing on ore bodies enriched in Cu. Physiologia Plantarum, 88(2), 307–314.

    Article  CAS  Google Scholar 

  • Lanquar, V., et al. (2010). Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiology, 152, 1986–1999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, J., Peña, M. M. O., Nose, Y., & Thiele, D. J. (2002). Biochemical characterization of the human copper transporter Ctr1. Journal of Biological Chemistry, 277(6), 4380–4387.

    Article  CAS  Google Scholar 

  • Lee, S., & An, G. (2009). Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant, Cell & Environment, 32(4), 408–416.

    Article  CAS  Google Scholar 

  • Lee, S., Chiecko, J. C., Kim, S. A., Walker, E. L., Lee, Y., Guerinot, M. L., & An, G. (2009a). Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiology, 150(2), 786–800.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Proceedings of the National Academy of Sciences, 106(51), 22014–22019.

    Article  CAS  Google Scholar 

  • Lee, S., Jeong, H. J., Kim, S. A., Lee, J., Guerinot, M. L., & An, G. (2010). OsZIP5 is a plasma membrane zinc transporter in rice. Plant Molecular Biology, 73(4-5), 507–517.

    Article  CAS  PubMed  Google Scholar 

  • Lee, S., Kim, Y. S., Jeon, U. S., Kim, Y. K., Schjoerring, J. K., & An, G. (2012). Activation of rice nicotianamine synthase 2 (OsNAS2) enhances iron availability for biofortification. Molecules and Cells, 33(3), 269–275.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, S., Kim, Y. Y., Lee, Y., & An, G. (2007). Rice P1B-type heavy-metal ATPase, OsHMA9, is a metal efflux protein. Plant Physiology, 145(3), 831–842.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. (2011). Bio-available zinc in rice seeds is increased by activation tagging of nicotianamine synthase. Plant Biotechnology Journal, 9(8), 865–873.

    Article  CAS  PubMed  Google Scholar 

  • Leitenmaier, B., & Küpper, H. (2013). Compartmentation and complexation of metals in hyperaccumulator plants. Frontiers in Plant Science, 4, 374.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li, H., Fan, R., Li, L., Wei, B. O., Li, G., Gu, L., Wang, X., & Zhang, X. (2014). Identification and characterization of a novel copper transporter gene family TaCT 1 in common wheat. Plant, Cell & Environment, 37(7), 1561–1573.

    Article  CAS  Google Scholar 

  • Li, L. Y., Cai, Q. Y., Yu, D. S., & Guo, C. H. (2011). Overexpression of AtFRO6 in transgenic tobacco enhances ferric chelate reductase activity in leaves and increases tolerance to iron-deficiency chlorosis. Molecular Biology Reports, 38(6), 3605–3613.

    Article  CAS  PubMed  Google Scholar 

  • Lombardi, L., & Sebastiani, L. (2005). Copper toxicity in Prunus cerasifera: Growth and antioxidant enzymes responses of in vitro grown plants. Plant Science, 168(3), 797–802.

    Article  CAS  Google Scholar 

  • López-Millán, A. F., Duy, D., & Philippar, K. (2016). Chloroplast iron transport proteins–function and impact on plant physiology. Frontiers in Plant Science, 7, 178.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lopez-Millan, A. F., Ellis, D. R., & Grusak, M. A. (2004). Identification and characterization of several new members of the ZIP family of metal ion transporters in Medicago truncatula. Plant Molecular Biology, 54(4), 583–596.

    Article  CAS  PubMed  Google Scholar 

  • Mansfeldt, T. (2004). Redox potential of bulk soil and soil solution concentration of nitrate, manganese, iron, and sulfate in two Gleysols. Journal of Plant Nutrition and Soil Science, 167(1), 7–16.

    Article  CAS  Google Scholar 

  • Marschner, H. (1995). Mineral nutrition of higher plants (2nd ed.). London: Academic Press.

    Google Scholar 

  • Marshall, J., Corzo, A., Leigh, R. A., & Sanders, D. (1994). Membrane potential-dependent calcium transport in right-side-out plasma membrane vesicles from Zea mays L. roots. The Plant Journal, 5(5), 683–694.

    Article  CAS  Google Scholar 

  • Masuda, H., Ishimaru, Y., Aung, M. S., Kobayashi, T., Kakei, Y., Takahashi, M., et al. (2012). Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition. Scientific Report, 2, 1–7. https://doi.org/10.1038/srep00543.

    Article  CAS  Google Scholar 

  • Masuda, H., Usuda, K., Kobayashi, T., Ishimaru, Y., Kakei, Y., Takahashi, M., Higuchi, K., Nakanishi, H., Mori, S., & Nishizawa, N. K. (2009). Overexpression of the barley nicotianamine synthase gene HvNAS1 increases iron and zinc concentrations in rice grains. Rice, 2(4), 155–166.

    Article  Google Scholar 

  • Migocka, M., & Malas, K. (2018). Plant responses to copper: Molecular and regulatory mechanisms of copper uptake, distribution and accumulation in plants. In Plant micronutrient use efficiency (pp. 71–86). London: Academic Press.

    Chapter  Google Scholar 

  • Miller, J. L. (2013). Iron deficiency anemia: A common and curable disease. Cold Spring Harbor Perspectives in Medicine, 3(7), a011866.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mills, R. F., Doherty, M. L., Lopez-Marques, R. L., Weimar, T., Dupree, P., Palmgren, M. G., et al. (2008). ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiology, 146, 116–128. https://doi.org/10.1104/pp.107.110817.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mira, H., Martínez-García, F., & Peñarrubia, L. (2001). Evidence for the plant-specific intercellular transport of the Arabidopsis copper chaperone CCH. The Plant Journal, 25(5), 521–528.

    Article  CAS  PubMed  Google Scholar 

  • Montanini, B., Blaudez, D., Jeandroz, S., Sanders, D., & Chalot, M. (2007). Phylogenetic and functional analysis of the cation diffusion facilitator (CDF) family: Improved signature and prediction of substrate specificity. BMC Genomics, 8(1), 107.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mori, S., & Nishizawa, N. (1987). Methionine as a dominant precursor of phytosiderophores in graminaceae: Plants. Plant Cell Physiology, 28, 1081–1092.

    CAS  Google Scholar 

  • Morrissey, J., & Guerinot, M. L. (2009). Iron uptake and transport in plants: The good, the bad, and the ionome. Chemical Reviews, 109(10), 4553–4567.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mukherjee, I., Campbell, N. H., Ash, J. S., & Connolly, E. L. (2006). Expression profiling of the Arabidopsis ferric chelate reductase (FRO) gene family reveals differential regulation by iron and copper. Planta, 223(6), 1178–1190.

    Article  CAS  PubMed  Google Scholar 

  • Müller, B., Kovács, K., Pham, H. D., Kavak, Y., Pechoušek, J., Machala, L., Zbořil, R., Szenthe, K., Abadía, J., Fodor, F., & Klencsár, Z. (2019). Chloroplasts preferentially take up ferric–citrate over iron–nicotianamine complexes in Brassica napus. Planta, 249(3), 751–763.

    Article  PubMed  CAS  Google Scholar 

  • Myers, S. S., Zanobetti, A., Kloog, I., Huybers, P., Leakey, A. D., Bloom, A. J., Carlisle, E., Dietterich, L. H., Fitzgerald, G., Hasegawa, T., & Holbrook, N. M. (2019). Increasing CO2 threatens human nutrition (vol 510, pg 139, 2014). Nature, 574(7778), E14–E14.

    Article  CAS  PubMed  Google Scholar 

  • Narayanan, N., Beyene, G., Chauhan, R. D., Gaitán-Solís, E., Gehan, J., Butts, P., Siritunga, D., Okwuonu, I., Woll, A., Jiménez-Aguilar, D. M., & Boy, E. (2019). Biofortification of field-grown cassava by engineering expression of an iron transporter and ferritin. Nature Biotechnology, 37(3), 323.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narayanan, N., Beyene, G., Chauhan, R. D., Gaitán-Solis, E., Grusak, M. A., Taylor, N., & Anderson, P. (2015). Overexpression of Arabidopsis VIT1 increases accumulation of iron in cassava roots and stems. Plant Science, 240, 170–181.

    Article  CAS  PubMed  Google Scholar 

  • Nekrasova, G. F., Ushakova, O. S., Ermakov, A. E., Uimin, M. A., & Byzov, I. V. (2011). Effects of copper (II) ions and copper oxide nanoparticles on Elodea densa Planch. Russian Journal of Ecology, 42(6), 458.

    Article  CAS  Google Scholar 

  • Nevo, Y., & Nelson, N. (2006). The NRAMP family of metal-ion transporters. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1763(7), 609–620.

    Article  CAS  Google Scholar 

  • Nozoye, T., Nagasaka, S., Bashir, K., Takahashi, M., Kobayashi, T., Nakanishi, H., & Nishizawa, N. K. (2014). Nicotianamine synthase 2 localizes to the vesicles of iron-deficient rice roots, and its mutation in the YXX φ or LL motif causes the disruption of vesicle formation or movement in rice. The Plant Journal, 77(2), 246–260.

    Article  CAS  PubMed  Google Scholar 

  • Nozoye, T., Nagasaka, S., Kobayashi, T., Sato, Y., Uozumi, N., Nakanishi, H., & Nishizawa, N. K. (2015). The phytosiderophore efflux transporter TOM2 is involved in metal transport in rice. Journal of Biological Chemistry, 290(46), 27688–27699.

    Article  CAS  Google Scholar 

  • Nozoye, T., Nagasaka, S., Kobayashi, T., Takahashi, M., Sato, Y., Sato, Y., Uozumi, N., Nakanishi, H., & Nishizawa, N. K. (2011). Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. Journal of Biological Chemistry, 286(7), 5446–5454. https://doi.org/10.1074/jbc.M110.180026.

    Article  CAS  Google Scholar 

  • Nunan, K. J., & Scheller, H. V. (2003). Solubilization of an arabinan arabinosyltransferase activity from mung bean hypocotyls. Plant Physiology, 132(1), 331–342.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogo, Y., Itai, R. N., Kobayashi, T., Aung, M. S., Nakanishi, H., & Nishizawa, N. K. (2011). OsIRO2 is responsible for iron utilization in rice and improves growth and yield in calcareous soil. Plant Molecular Biology, 75(6), 593–605.

    Article  CAS  PubMed  Google Scholar 

  • Oliva, N., Chadha-Mohanty, P., Poletti, S., Abrigo, E., Atienza, G., Torrizo, L., Garcia, R., Dueñas, C., Poncio, M. A., Balindong, J., & Manzanilla, M. (2014). Large-scale production and evaluation of marker-free indica rice IR64 expressing phytoferritin genes. Molecular Breeding, 33(1), 23–37.

    Article  CAS  PubMed  Google Scholar 

  • Oono, Y., Yazawa, T., Kawahara, Y., Kanamori, H., Kobayashi, F., Sasaki, H., Mori, S., Wu, J., Handa, H., Itoh, T., & Matsumoto, T. (2014). Genome-wide transcriptome analysis reveals that cadmium stress signaling controls the expression of genes in drought stress signal pathways in rice. PLoS One, 9(5), e96946.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oparka, K. J., & Gates, P. (1984). Sink anatomy in relation to solute movement in rice (Oryza sativa L.): A summary of findings. Plant Growth Regulation, 2(4), 297–307.

    Article  CAS  Google Scholar 

  • Page, V., Le Bayon, R. C., & Feller, U. (2006). Partitioning of zinc, cadmium, manganese and cobalt in wheat (Triticum aestivum) and lupin (Lupinus albus) and further release into the soil. Environmental and Experimental Botany, 58(1-3), 269–278.

    Article  CAS  Google Scholar 

  • Palmgren, M. G., Clemens, S., Williams, L. E., Krämer, U., Borg, S., Schjørring, J. K., & Sanders, D. (2008). Zinc biofortification of cereals: Problems and solutions. Trends in Plant Science, 13(9), 464–473.

    Article  CAS  PubMed  Google Scholar 

  • Pedas, P., Ytting, C. K., Fuglsang, A. T., Jahn, T. P., Schjoerring, J. K., & Husted, S. (2008). Manganese efficiency in barley: Identification and characterization of the metal ion transporter HvIRT1. Plant Physiology, 148(1), 455–466.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira, M. P., Santos, C., Gomes, A., & Vasconcelos, M. W. (2014). Cultivar variability of iron uptake mechanisms in rice (Oryza sativa L.). Plant Physiology and Biochemistry, 85, 21–30.

    Article  CAS  PubMed  Google Scholar 

  • Pfeiffer, W. H., & McClafferty, B. (2007). HarvestPlus: Breeding crops for better nutrition. Crop Science, 47(Supplement_3), S88–S105.

    Article  Google Scholar 

  • Pich, A., Manteuffel, R., Hillmer, S., Scholz, G., & Schmidt, W. (2001). Fe homeostasis in plant cells: Does nicotianamine play multiple roles in the regulation of cytoplasmic Fe concentration? Planta, 213(6), 967–976.

    Article  CAS  PubMed  Google Scholar 

  • Pike, M. M., Stoops, C. N., Langford, C. P., Akella, N. S., Nabors, L. B., & Gillespie, G. Y. (2009). High-resolution longitudinal assessment of flow and permeability in mouse glioma vasculature: Sequential small molecule and SPIO dynamic contrast agent MRI. Magnetic Resonance in Medicine: An Official Journal of the International Society for Magnetic Resonance in Medicine, 61(3), 615–625.

    Article  CAS  Google Scholar 

  • Pilon, M., Abdel-Ghany, S. E., Cohu, C. M., Gogolin, K. A., & Ye, H. (2006). Copper cofactor delivery in plant cells. Current Opinion in Plant Biology, 9(3), 256–263.

    Article  CAS  PubMed  Google Scholar 

  • Pineros, M. A., & Kochian, L. V. (2003). Differences in whole-cell and single-channel ion currents across the plasma membrane of mesophyll cells from two closely related Thlaspi species. Plant Physiology, 131(2), 583–594.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pirson, A., Tichy, C., & Wilhelmi, G. (1951). Metabolism and mineral salt diet unicellular green algae. Planta, 40, 199–253.

    Article  Google Scholar 

  • Pittman, J. K. (2005). Managing the manganese: Molecular mechanisms of manganese transport and homeostasis. New Phytology, 167, 733–742.

    Article  CAS  Google Scholar 

  • Prasad, T. N. V. K. V., Sudhakar, P., Sreenivasulu, Y., Latha, P., Munaswamy, V., Reddy, K. R., Sreeprasad, T. S., Sajanlal, P. R., & Pradeep, T. (2012). Effect of nanoscale zinc oxide particles on the germination, growth and yield of peanut. Journal of Plant Nutrition, 35(6), 905–927.

    Article  CAS  Google Scholar 

  • Puig, S., Andrés-Colás, N., García-Molina, A., & Peñarrubia, L. (2007). Copper and iron homeostasis in Arabidopsis: Responses to metal deficiencies, interactions and biotechnological applications. Plant, Cell & Environment, 30(3), 271–290.

    Article  CAS  Google Scholar 

  • Raboy, V. (2009). Approaches and challenges to engineering seed phytate and total phosphorus. Plant Science, 177(4), 281–296.

    Article  CAS  Google Scholar 

  • Radisky, D., & Kaplan, J. (1999). Regulation of transition metal transport across the yeast plasma membrane. Journal of Biological Chemistry, 274(8), 4481–4484.

    Article  CAS  Google Scholar 

  • Ramesh, S. A., Shin, R., Eide, D. J., & Schachtman, D. P. (2003). Differential metal selectivity and gene expression of two zinc transporters from rice. Plant Physiology, 133(1), 126–134.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rempel, S., Stanek, W. K., & Slotboom, D. J. (2018). Energy-coupling factor-type ATP-binding cassette transporters. Annual Review of Biochemistry, 88, 551–576.

    Article  CAS  Google Scholar 

  • Rengel, Z. (2000). Manganese uptake and transport in plants. In Metal ions in biological systems (pp. 105–136). Boca Raton: CRC Press.

    Google Scholar 

  • Ricachenevsky, F. K., & Sperotto, R. A. (2014). There and back again, or always there? The evolution of rice combined strategy for Fe uptake. Frontiers in Plant Science, 5, 189.

    Article  PubMed  PubMed Central  Google Scholar 

  • Robinson, N. J., Procter, C. M., Connolly, E. L., & Guerinot, M. L. (1999). A ferric-chelate reductase for iron uptake from soils. Nature, 397(6721), 694.

    Article  CAS  PubMed  Google Scholar 

  • Roschzttardtz, H., Conéjéro, G., Divol, F., Alcon, C., Verdeil, J. L., Curie, C., & Mari, S. (2013). New insights into Fe localization in plant tissues. Frontiers in Plant Science, 4, 350.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rose, T. J., Impa, S. M., Rose, M. T., Pariasca-Tanaka, J., Mori, A., Heuer, S., Johnson-Beebout, S. E., & Wissuwa, M. (2012). Enhancing phosphorus and zinc acquisition efficiency in rice: A critical review of root traits and their potential utility in rice breeding. Annals of Botany, 112(2), 331–345.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rutherford, A. W., & Boussac, A. (2004). Water photolysis in biology. Science, 303(5665), 1782–1784.

    Article  CAS  PubMed  Google Scholar 

  • Santi, S., & Schmidt, W. (2009). Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytologist, 183(4), 1072–1084.

    Article  CAS  Google Scholar 

  • Sasaki, A., Yamaji, N., & Ma, J. F. (2016). Transporters involved in mineral nutrient uptake in rice. Journal of Experimental Botany, 67(12), 3645–3653.

    Article  CAS  PubMed  Google Scholar 

  • Sasaki, A., Yamaji, N., Mitani-Ueno, N., Kashino, M., & Ma, J. F. (2015). A node-localized transporter Os ZIP 3 is responsible for the preferential distribution of Zn to developing tissues in rice. The Plant Journal, 84(2), 374–384.

    Article  CAS  PubMed  Google Scholar 

  • Sasaki, A., Yamaji, N., Xia, J., & Ma, J. F. (2011). OsYSL6 is involved in the detoxification of excess manganese in rice. Plant Physiology, 157(4), 1832–1840.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki, A., Yamaji, N., Yokosho, K., & Ma, J. F. (2012). Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. The Plant Cell, 24(5), 2155–2167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satoh-Nagasawa, N., Mori, M., Nakazawa, N., Kawamoto, T., Nagato, Y., Sakurai, K., Takahashi, H., Watanabe, A., & Akagi, H. (2011). Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant and Cell Physiology, 53(1), 213–224.

    Article  PubMed  CAS  Google Scholar 

  • Schiller, M., Hegelund, J. N., Pedas, P., Kichey, T., Laursen, K. H., Husted, S., & Schjoerring, J. K. (2014). Barley metallothioneins differ in ontogenetic pattern and response to metals. Plant, Cell & Environment, 37(2), 353–367.

    Article  CAS  Google Scholar 

  • Schnell Ramos, M., Khodja, H., Mary, V., & Thomine, S. (2013). Using μPIXE for quantitative mapping of metal concentration in Arabidopsis thaliana seeds. Frontiers in Plant Science, 4, 168.

    Article  PubMed  PubMed Central  Google Scholar 

  • Senoura, T., Sakashita, E., Kobayashi, T., Takahashi, M., Aung, M. S., Masuda, H., Nakanishi, H., & Nishizawa, N. K. (2017). The iron-chelate transporter OsYSL9 plays a role in iron distribution in developing rice grains. Plant Molecular Biology, 95(4-5), 375–387.

    Article  CAS  PubMed  Google Scholar 

  • Shao, J. F., Xia, J., Yamaji, N., Shen, R. F., & Ma, J. F. (2018). Effective reduction of cadmium accumulation in rice grain by expressing OsHMA3 under the control of the OsHMA2 promoter. Journal of Experimental Botany, 69(10), 2743–2752.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shenker, M., & Chen, Y. (2005). Increasing iron availability to crops: Fertilizers, organo-fertilizers, and biological approaches. Soil Science & Plant Nutrition, 51(1), 1–17.

    Article  CAS  Google Scholar 

  • Shenker, M., Plessner, O. E., & Tel-Or, E. (2004). Manganese nutrition effects on tomato growth, chlorophyll concentration, and superoxide dismutase activity. Journal of Plant Physiology, 161(2), 197–202.

    Article  CAS  PubMed  Google Scholar 

  • Shigaki, T., & Hirschi, K. D. (2006). Diverse functions and molecular properties emerging for CAX cation/H+ exchangers in plants. Plant Biology, 8(04), 419–429.

    Article  CAS  PubMed  Google Scholar 

  • Singh, A., Singh, N. B., Afzal, S., Singh, T., & Hussain, I. (2018). Zinc oxide nanoparticles: A review of their biological synthesis, antimicrobial activity, uptake, translocation and biotransformation in plants. Journal of Materials Science, 53(1), 185–201.

    Article  CAS  Google Scholar 

  • Socha, A. L., & Guerinot, M. L. (2014). Mn-euvering manganese: The role of transporter gene family members in manganese uptake and mobilization in plants. Frontiers in Plant Science, 5, 106.

    Article  PubMed  PubMed Central  Google Scholar 

  • Solti, Á., Müller, B., Czech, V., Sárvári, É., & Fodor, F. (2014). Functional characterization of the chloroplast ferric chelate oxidoreductase enzyme. New Phytologist, 202(3), 920–928.

    Article  CAS  Google Scholar 

  • Spector, M., & Winget, G. D. (1980). Purification of a manganese-containing protein involved in photosynthetic oxygen evolution and its use in reconstituting an active membrane. Proceedings of the National Academy of Sciences, 77(2), 957–959.

    Article  CAS  Google Scholar 

  • Sperotto, R. A., Ricachenevsky, F. K., Williams, L. E., Vasconcelos, M. W., & Menguer, P. K. (2014). From soil to seed: Micronutrient movement into and within the plant. Frontiers in Plant Science, 5, 438.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stein, R. J., Ricachenevsky, F. K., & Fett, J. P. (2009). Differential regulation of the two rice ferritin genes (OsFER1 and OsFER2). Plant Science, 177(6), 563–569.

    Article  CAS  Google Scholar 

  • Stephan, U. W., Schmidke, I., & Pich, A. (1994). Phloem translocation of Fe, Cu, Mn, and Zn in Ricinus seedlings in relation to the concentrations of nicotianamine, an endogenous chelator of divalent metal ions, in different seedling parts. Plant and Soil, 165(2), 181–188.

    Article  CAS  Google Scholar 

  • Stephan, U. W., & Scholz, G. (1993). Nicotianamine: Mediator of transport of iron and heavy metals in the phloem? Physiologia Plantarum, 88(3), 522–529.

    Article  CAS  Google Scholar 

  • Suzuki, M., Bashir, K., Inoue, H., Takahashi, M., Nakanishi, H., & Nishizawa, N. K. (2012). Accumulation of starch in Zn-deficient rice. Rice, 5(1), 9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Suzuki, M., Takahashi, M., Tsukamoto, T., Watanabe, S., Matsuhashi, S., Yazaki, J., Kishimoto, N., Kikuchi, S., Nakanishi, H., Mori, S., & Nishizawa, N. K. (2006). Biosynthesis and secretion of mugineic acid family phytosiderophores in zinc-deficient barley. The Plant Journal, 48(1), 85–97.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, M., Tsukamoto, T., Inoue, H., Watanabe, S., Matsuhashi, S., Takahashi, M., Nakanishi, H., Mori, S., & Nishizawa, N. K. (2008). Deoxymugineic acid increases Zn translocation in Zn-deficient rice plants. Plant Molecular Biology, 66(6), 609–617.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi, M., Terada, Y., Nakai, I., Nakanishi, H., Yoshimura, E., Mori, S., & Nishizawa, N. K. (2003). Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. The Plant Cell, 15(6), 1263–1280. https://doi.org/10.1105/tpc.010256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi, R., Ishimaru, Y., Shimo, H., Ogo, Y., Senoura, T., Nishizawa, N. K., & Nakanishi, H. (2012). The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant, Cell & Environment, 35(11), 1948–1957.

    Article  CAS  Google Scholar 

  • Takemoto, Y., Tsunemitsu, Y., Fujii-Kashino, M., Mitani-Ueno, N., Yamaji, N., Ma, J. F., S-i, K., Iwasaki, K., & Ueno, D. (2017). The tonoplast-localized transporter MTP8.2 contributes to manganese detoxification in the shoots and roots of Oryza sativa L. Plant Cell Physiology, 58(9), 1573–1582. https://doi.org/10.1093/pcp/pcx082.

    Article  CAS  PubMed  Google Scholar 

  • Talke, I. N., Hanikenne, M., & Krämer, U. (2006). Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiology, 142(1), 148–167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tauris, B., Borg, S., Gregersen, P. L., & Holm, P. B. (2009). A roadmap for zinc trafficking in the developing barley grain based on laser capture microdissection and gene expression profiling. Journal of Experimental Botany, 60(4), 1333–1347.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tolay, I., Erenoglu, B., Römheld, V., Braun, H. J., & Cakmak, I. (2001). Phytosiderophore release in Aegilops tauschii and Triticum species under zinc and iron deficiencies. Journal of Experimental Botany, 52(358), 1093–1099.

    Article  CAS  PubMed  Google Scholar 

  • Tsai, H. H., Rodriguez-Celma, J., Lan, P., Wu, Y. C., Vélez-Bermúdez, I. C., & Schmidt, W. (2018). Scopoletin 8-hydroxylase-mediated fraxetin production is crucial for iron mobilization. Plant Physiology, 177(1), 194–207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsukamoto, T., Nakanishi, H., Uchida, H., Watanabe, S., Matsuhashi, S., Mori, S., & Nishizawa, N. K. (2008). 52Fe translocation in barley as monitored by a positron-emitting tracer imaging system (PETIS): Evidence for the direct translocation of Fe from roots to young leaves via phloem. Plant and Cell Physiology, 50(1), 48–57.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tsunemitsu, Y., Genga, M., Okada, T., Yamaji, N., Ma, J. F., Miyazaki, A., Kato, S. I., Iwasaki, K., & Ueno, D. (2018). A member of cation diffusion facilitator family, MTP11, is required for manganese tolerance and high fertility in rice. Planta, 248(1), 231–241.

    Article  CAS  PubMed  Google Scholar 

  • Ueno, D., Sasaki, A., Yamaji, N., Miyaji, T., Fujii, Y., Takemoto, Y., Moriyama, S., Che, J., Moriyama, Y., Iwasaki, K., & Ma, J. F. (2015). A polarly localized transporter for efficient manganese uptake in rice. Nature Plants, 1(12), 15170.

    Article  CAS  PubMed  Google Scholar 

  • Vasconcelos, M., Datta, K., Oliva, N., Khalekuzzaman, M., Torrizo, L., Krishnan, S., Oliveira, M., Goto, F., & Datta, S. K. (2003). Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. Plant Science, 164(3), 371–378.

    Article  CAS  Google Scholar 

  • Vert, G., Grotz, N., Dédaldéchamp, F., Gaymard, F., Guerinot, M. L., Briat, J. F., & Curie, C. (2002). IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. The Plant Cell, 14(6), 1223–1233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vigani, G., Rolli, E., Marasco, R., Dell’Orto, M., Michoud, G., Soussi, A., Raddadi, N., Borin, S., Sorlini, C., Zocchi, G., & Daffonchio, D. (2019). Root bacterial endophytes confer drought resistance and enhance expression and activity of a vacuolar H+-pumping pyrophosphatase in pepper plants. Environmental Microbiology, 21(9), 3212–3228.

    Article  CAS  Google Scholar 

  • Vigani, G., Zocchi, G., Bashir, K., Philippar, K., & Briat, J. F. (2013). Signals from chloroplasts and mitochondria for iron homeostasis regulation. Trends in Plant Science, 18(6), 305–311.

    Article  CAS  PubMed  Google Scholar 

  • Waters, B. M., Blevins, D. G., & Eide, D. J. (2002). Characterization of FRO1, a pea ferric-chelate reductase involved in root iron acquisition. Plant Physiology, 129(1), 85–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waters, B. M., Chu, H. H., DiDonato, R. J., Roberts, L. A., Eisley, R. B., Lahner, B., Salt, D. E., & Walker, E. L. (2006). Mutations in Arabidopsis yellow stripe-like1 and yellow stripe-like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiology, 141(4), 1446–1458.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waters, B. M., & Grusak, M. A. (2008). Whole-plant mineral partitioning throughout the life cycle in Arabidopsis thaliana ecotypes Columbia, Landsberg erecta, Cape Verde Islands, and the mutant line ysl1ysl3. New Phytologist, 177(2), 389–405.

    Google Scholar 

  • Waters, B. M., Lucena, C., Romera, F. J., Jester, G. G., Wynn, A. N., Rojas, C. L., Alcántara, E., & Pérez-Vicente, R. (2007). Ethylene involvement in the regulation of the H+-ATPase CsHA1 gene and of the new isolated ferric reductase CsFRO1 and iron transporter CsIRT1 genes in cucumber plants. Plant Physiology and Biochemistry, 45(5), 293–301.

    Article  CAS  PubMed  Google Scholar 

  • Waters, B. M., & Sankaran, R. P. (2011). Moving micronutrients from the soil to the seeds: Genes and physiological processes from a biofortification perspective. Plant Science, 180(4), 562–574.

    Article  CAS  PubMed  Google Scholar 

  • White, P. J., & Broadley, M. R. (2009). Biofortification of crops with seven mineral elements often lacking in human diets–iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytologist, 182(1), 49–84.

    Article  CAS  Google Scholar 

  • Wintz, H., Fox, T., Wu, Y. Y., Feng, V., Chen, W., Chang, H. S., Zhu, T., & Vulpe, C. (2003). Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. Journal of Biological Chemistry, 278(48), 47644–47653.

    Article  CAS  Google Scholar 

  • Wissemeier, A. H., & Horst, W. J. (1987). Callose deposition in leaves of cowpea (Vigna unguiculata (L.) Walp.) as a sensitive response to high Mn supply. Plant and Soil, 102, 283–286.

    Article  CAS  Google Scholar 

  • Wong, C. K., Jarvis, R. S., Sherson, S. M., & Cobbett, C. S. (2009). Functional analysis of the heavy metal binding domains of the Zn/Cd-transporting ATPase, HMA2, in Arabidopsis thaliana. New Phytology, 181, 79–88. https://doi.org/10.1111/j.1469-8137.2008.02637.x.

    Article  CAS  Google Scholar 

  • Wong, C. K. E., & Cobbett, C. S. (2009). HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytologist, 181(1), 71–78.

    Article  CAS  Google Scholar 

  • Wu, L. B., Ueda, Y., Lai, S. K., & Frei, M. (2016). Shoot tolerance mechanisms to iron toxicity in rice (Oryza sativa L.). Plant, Cell & Environment, 40(4), 570–584.

    Article  CAS  Google Scholar 

  • Wu, T., Kamiya, T., Yumoto, H., Sotta, N., Katsushi, Y., Shigenobu, S., Matsubayashi, Y., & Fujiwara, T. (2015). An Arabidopsis thaliana copper-sensitive mutant suggest a role of phytosulfokine in ethylene production. Journal of Experimental Botany, 66, 3657–3667. https://doi.org/10.1093/jxb/erv105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, T. Y., Gruissem, W., & Bhullar, N. K. (2019). Targeting intracellular transport combined with efficient uptake and storage significantly increases grain iron and zinc levels in rice. Plant Biotechnology Journal, 17(1), 9–20.

    Article  CAS  PubMed  Google Scholar 

  • Xu, X., Cao, X., Zhao, L., Wang, H., Yu, H., & Gao, B. (2013). Removal of Cu, Zn, and Cd from aqueous solutions by the dairy manure-derived biochar. Environmental Science and Pollution Research, 20(1), 358–368.

    Article  CAS  PubMed  Google Scholar 

  • Yamaji, N., & Ma, J. F. (2014). The node, a hub for mineral nutrient distribution in graminaceous plants. Trends in Plant Science, 19(9), 556–563.

    Article  CAS  PubMed  Google Scholar 

  • Yamaji, N., Sasaki, A., Xia, J. X., Yokosho, K., & Ma, J. F. (2013a). A node-based switch for preferential distribution of manganese in rice. Nature Communications, 4, 2442.

    Article  PubMed  CAS  Google Scholar 

  • Yamaji, N., Xia, J., Mitani-Ueno, N., Yokosho, K., & Ma, J. F. (2013b). Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiology, 162(2), 927–939.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, A., & Zhang, W. H. (2016). A small GTPase, OsRab6q, is involved in the regulation of iron homeostasis in rice. Plant Cell Physiology, 57, 1271–1280. https://doi.org/10.1093/jxb/erq301.

    Article  CAS  PubMed  Google Scholar 

  • Yang, M., Zhang, Y., Zhang, L., Hu, J., Zhang, X., Lu, K., Dong, H., Wang, D., Zhao, F. J., Huang, C. F., & Lian, X. (2014). OsNRAMP5 contributes to manganese translocation and distribution in rice shoots. Journal of Experimental Botany, 65(17), 4849–4861.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, Z., Wu, Y., Li, Y., Ling, H. Q., & Chu, C. (2009). OsMT1a, a type 1 metallothionein, plays the pivotal role in zinc homeostasis and drought tolerance in rice. Plant Molecular Biology, 70(1–2), 219–229.

    Article  CAS  PubMed  Google Scholar 

  • Yen, M. R., Tseng, Y. H., & Saier, M. H., Jr. (2001). Maize Yellow Stripe1, an iron-phytosiderophore uptake transporter, is a member of the oligopeptide transporter (OPT) family. Microbiology, 147(11), 2881–2883.

    Article  CAS  PubMed  Google Scholar 

  • Yokosho, K., Yamaji, N., & Ma, J. F. (2016). OsFRDL1 expressed in nodes is required for distribution of iron to grains in rice. Journal of Experimental Botany, 67(18), 5485–5494.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoneyama, T., Ishikawa, S., & Fujimaki, S. (2015). Route and regulation of zinc, cadmium, and iron transport in rice plants (Oryza sativa L.) during vegetative growth and grain filling: Metal transporters, metal speciation, grain Cd reduction and Zn and Fe biofortification. International Journal of Molecular Sciences, 16(8), 19111–19129.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yruela, I. (2005). Copper in plants. Brazilian Journal of Plant Physiology, 17(1), 145–156. https://doi.org/10.1590/S1677-04202005000100012.

    Article  CAS  Google Scholar 

  • Yuan, M., Li, X., Xiao, J., & Wang, S. (2011). Molecular and functional analyses of COPT/Ctr-type copper transporter-like gene in family in rice. BMC Plant Biology, 11, 69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhai, Z., Gayomba, S. R., Jung, H. I., Vimalakumari, N. K., Piñeros, M., Craft, E., Rutzke, M. A., Danku, J., Lahner, B., Punshon, T., & Guerinot, M. L. (2014). OPT3 is a phloem-specific iron transporter that is essential for systemic iron signaling and redistribution of iron and cadmium in Arabidopsis. The Plant Cell, 26(5), 2249–2264.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, W. H., Zhou, Y., Dibley, K. E., Tyerman, S. D., Furbank, R. T., & Patrick, J. W. (2007). Nutrient loading of developing seeds. Functional Plant Biology, 34(4), 314–331.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Y., Xu, Y. H., Yi, H. Y., & Gong, J. M. (2012). Vacuolar membrane transporters OsVIT1 and OsVIT2 modulate iron translocation between flag leaves and seeds in rice. The Plant Journal, 72(3), 400–410.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, L., Yamaji, N., Yokosho, K., & Ma, J. F. (2012). YSL16 is a phloem-localized transporter of the copper-nicotianamine complex that is responsible for copper distribution in rice. The Plant Cell, 24(9), 3767–3782.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, W., Zuo, R., Zhou, R., Huang, J., Tang, M., Cheng, X., Liu, Y., Tong, C., Xiang, Y., Dong, C., & Liu, S. (2016). Vacuolar iron transporter BnMEB2 is involved in enhancing iron tolerance of Brassica napus. Frontiers in Plant Science, 7, 1353.

    PubMed  PubMed Central  Google Scholar 

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  1. Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India

    Shadma Afzal, Preeti Sirohi, Deepa Sharma & Nand K. Singh

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  1. Shadma Afzal
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  1. Department of Botany, Aligarh Muslim University, Aligarh, India

    Tariq Aftab

  2. Department of Biological Sciences, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia

    Khalid Rehman Hakeem

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Afzal, S., Sirohi, P., Sharma, D., Singh, N.K. (2020). Micronutrient Movement and Signalling in Plants from a Biofortification Perspective. In: Aftab, T., Hakeem, K.R. (eds) Plant Micronutrients. Springer, Cham. https://doi.org/10.1007/978-3-030-49856-6_7

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