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Genetic Engineering and Molecular Strategies for Nutrient Manipulation in Plants

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Essential Plant Nutrients

Abstract

Plants require an adequate balance of mineral nutrients in each stage of development to achieve maximum yield. Deficiencies of mineral nutrients are common in crops worldwide. To solve this problem in modern agriculture, the fertilizer applications are necessary, but this practice may be associated with undesirable environmental impacts as well as the high cost of fertilizers. However, improving nutrient use efficiency (NUE) via genetic manipulation may result in increased plant capacity to capture and utilize nutrients. In this chapter, we presented the advances made through genetic engineering and molecular strategies in a range of plant species aimed at enhancing uptake, translocation, and remobilization of nutrients as a sustainable way to increase crop productivity and quality.

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References

  • Abdulnour, J. E., Donnelly, D. J., & Barthakur, N. N. (2000). The effect of boron on calcium uptake and growth in micropropagated potato plantlets. Potato Research, 43, 287–295.

    Article  CAS  Google Scholar 

  • Abhishek, B., Sahrawat, K. L., Shiv, K., Rohit, J., Parihar, A. K., Ummed, S., Deepak, S., & Singh, N. P. (2015). Genetics- and genomics-based interventions for nutritional enhancement of grain legume crops: Status and outlook. Journal of Applied Genetics, 56, 151–161.

    Article  CAS  Google Scholar 

  • Ai, P., Sun, S., Zhao, J., Fan, X., **n, W., Guo, Q., Yu, L., Shen, Q., Wu, P., Miller, A. J., & Xu, G. (2009). Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. The Plant Journal, 57, 798–780.

    Article  CAS  PubMed  Google Scholar 

  • Almagro, A., Lin, S. H., & Tsay, Y. F. (2008). Characterization of the Arabidopsis nitrate transporter NRT1.6 reveals a role of nitrate in early embryo development. Plant Cell, 20, 3289–3299.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson, J. A., Huprikar, S. S., Kochian, L. V., Lucas, W. J., & Gaber, R. F. (1992). Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America, 89, 3736–3740.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arpat, A. B., Magliano, P., Wege, S., Rouached, H., Stefanovic, A., & Poirier, Y. (2012). Functional expression of PHO1 to the Golgi and trans-golgi network and its role in export of inorganic phosphate. The Plant Journal, 71, 479–491.

    CAS  PubMed  Google Scholar 

  • Asad, A., Bell, R., Dell, B., & Huang, L. (1997). Development of a boron buffered solution culture system for studying plant boron nutrition. Plant and Soil, 188, 21–32.

    Article  CAS  Google Scholar 

  • Assuncao, A. G., Herrero, E., Lin, Y. F., Huettel, B., Talukdar, S., Smaczniak, C., Immink, R. G. H., van Eldike, M., Fierse, M., Schat, H., & Aarts, M. G. M. (2010). Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency. Proceedings of the National Academy of Sciences of the United States of America, 107, 10296–10301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ayadi, A., David, P., Arrighi, J. F., Chiarenza, S., Thibaud, M. C., Nussaume, L., & Marin, E. (2015). Reducing the genetic redundancy of Arabidopsis PHOSPHATE TRANSPORTER1 transporters to study phosphate uptake and signaling. Plant Physiology, 167, 1511–1526.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baas, R., Van Oers, S., Silber, A., Bernstein, N., Ioffe, M., Keinan, M., & Bar-Tal, A. (2003). Calcium distribution in cut roses as related to transpiration. The Journal of Horticultural Science and Biotechnology, 78, 1–9.

    Article  CAS  Google Scholar 

  • Baldwin, J. C., Karthikeyan, A. S., Cao, A., & Raghothama, K. G. (2008). Biochemical and molecular analysis of LePS2;1: A phosphate starvation induced protein phosphatase gene from tomato. Planta, 228, 273–280.

    Article  CAS  PubMed  Google Scholar 

  • Barragán, V., Leidi, E. O., Andrés, Z., Rubio, L., De Luca, A., Fernández, J. A., Cubero, B., & Pardo, J. M. (2012). Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell, 24, 1127–1142.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bashir, K., Nozoye, T., Ishimaru, Y., Nakanishi, H., & Nishizawa, N. K. (2013). Exploiting new tools for iron bio-fortification of rice. Biotechnology Advances, 31, 1624–1633.

    Article  CAS  PubMed  Google Scholar 

  • Bassil, E., Tajima, H., Liang, Y. C., Ohto, M. A., Ushijima, K., Nakano, R., Esumi, T., Coku, A., Belmonte, M., & Blumwald, E. (2011). The Arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. Plant Cell, 23, 3482–3497.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berezin, I., Mizrachy-Dagry, T., Brook, E., Mizrahi, K., Elazar, M., Zhuo, S., Saul-Tcherkas, V., & Shaul, O. (2008). Overexpression of AtMHX in tobacco causes increased sensitivity to Mg2+, Zn2+, and Cd2+ ions, induction of V-ATPase expression, and a reduction in plant size. Plant Cell Reports, 27, 939–949.

    Article  CAS  PubMed  Google Scholar 

  • Borlaug, N. (1983). Contributions of conventional plant breeding to food production. Science, 219, 689–693.

    Article  CAS  PubMed  Google Scholar 

  • Bose, J., Babourina, O., Shabala, S., & Rengel, Z. (2013). Low-pH and aluminum resistance in Arabidopsis correlates with high cytosolic magnesium content and increased magnesium uptake by plant roots. Plant & Cell Physiology, 54, 1093–1104.

    Article  CAS  Google Scholar 

  • Bose, J., Rodrigo-Moreno, A., & Shabala, S. (2014). ROS homeostasis in halophytes in the context of salinity stress tolerance. Journal of Experimental Botany, 65, 1241–1257.

    Article  CAS  PubMed  Google Scholar 

  • Bose, J., Rodrigo-Moreno, A., Lai, D., **e, Y., Shen, W., & Shabala, S. (2015). Rapid regulation of the plasma membrane H1-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Annals of Botany, 115, 481–494.

    Article  PubMed  Google Scholar 

  • Brown, P. H., Bellaloui, N., Hu, H., & Dandekar, A. (1999). Transgenically enhanced sorbitol synthesis facilitates phloem boron transport and increases tolerance of tobacco to boron deficiency. Plant Physiology, 119, 17–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown, P. H., Bellaloui, N., Wimmer, M. A., Bassil, E. S., Ruiz, J., Hu, H., Pfeffer, H., Dannel, F., & Romheld, V. (2002). Boron in plant biology. Plant Biology, 4, 205–223.

    Article  CAS  Google Scholar 

  • Buchner, P., Stuiver, C. E. E., Westerman, S., Wirtz, M., Hell, R., Hawkesford, M. J., & De Kok, L. J. (2004). Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea as affected by atmospheric H2S and pedospheric sulfate nutrition. Plant Physiology, 136, 3396–3408.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bui, D. M., Gregan, J., Jarosch, E., Ragnini, A., & Schweyen, R. J. (1999). The bacterial magnesium transporter CorA can functionally substitute for its putative homologue Mrs2p in the yeast inner mitochondrial membrane. The Journal of Biological Chemistry, 274, 20438–20443.

    Article  CAS  PubMed  Google Scholar 

  • Burkhead, J. L., Reynolds, K. A., Abdel-Ghany, S. E., Cohu, C. M., & Pilon, M. (2009). Copper homeostasis. The New Phytologist, 182, 799–816.

    Article  CAS  PubMed  Google Scholar 

  • Byrne, S. L., Foito, A., Hedley, P. E., Morris, J. A., Stewart, D., & Barth, S. (2011). Early response mechanisms of perennial ryegrass (Lolium perenne) to phosphorus deficiency. Annals of Botany, 107, 243–254.

    Article  CAS  PubMed  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. Plant Cell, 22, 904–917.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cakmak, I. (2013). Magnesium in crop production, food quality and human health. Plant and Soil, 368, 1–4.

    Article  CAS  Google Scholar 

  • Cakmak, I., & Yazici, A. (2010). Magnesium: A forgotten element in crop production. Better Crops, 94, 1–3.

    Google Scholar 

  • Cañon, P., Aquea, F., Rodríguez-Hoces de la Guardia, A., & Arce-Johnson, P. (2013). Functional characterization of Citrus macrophylla BOR1 as a boron transporter. Physiologia Plantarum, 149, 329–339.

    PubMed  Google Scholar 

  • Castiglioni, S., Cazzaniga, A., Albisetti, W., & Maier, J. (2013). Magnesium and osteoporosis: Current state of knowledge and future research directions. Nutrients, 5, 3022–3033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cellier, F., Conéjéro, G., Ricaud, L., Luu, D. T., Lepetit, M., Gosti, F., & Casse, F. (2004). Characterization of AtCHX17, a member of the cation/H+ exchangers, CHX family, from Arabidopsis thaliana suggests a role in K+ homeostasis. The Plant Journal, 39, 834–846.

    Article  CAS  PubMed  Google Scholar 

  • Chen, Z., & Ma, J. (2013). Magnesium transporters and their role in Al tolerance in plants. Plant and Soil, 368, 51–56.

    Article  CAS  Google Scholar 

  • Chen, Z., Yamaji, N., Motoyama, R., Nagamura, Y., & Ma, J. (2012). Up-regulation of a magnesium transporter gene OsMGT1 is required for conferring aluminum tolerance in rice. Plant Physiology, 159, 1624–1633.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng, C., & Rerkasem, B. (1993). Effects of boron on pollen viability in wheat. Plant and Soil, 155, 313–315.

    Article  Google Scholar 

  • Chiu, C. C., Lin, C. S., Hsia, A. P., RC, S., Lin, H. L., & Tsay, Y. F. (2004). Mutation of a nitrate transporter, AtNRT1:4, results in a reduced petiole nitrate content and altered leaf development. Plant & Cell Physiology, 45, 1139–1148.

    Article  CAS  Google Scholar 

  • Clarkson, D. T. (1985). Factors affecting mineral nutrient acquisition by plants. Annual Review of Plant Physiology, 36, 77–115.

    Article  CAS  Google Scholar 

  • Cong, Y. X., Luo, D. F., Chen, K. M., Jiang, L. X., & Guo, W. L. (2012). The development of magnesium transport systems in organisms. Journal of Agricultural Biotechnology, 20, 837–848.

    CAS  Google Scholar 

  • Connolly, E. L., Campbell, N. H., Grotz, N., Prichard, C. L., & Guerinot, M. L. (2003). Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiology, 133, 1102–1110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Connolly, E. L. (2008). Raising the bar for biofortification: Enhanced levels of bioavailable calcium in carrots. Trends in Biotechnology, 26, 401–403.

    Google Scholar 

  • Correia, C. M., Moutinho Pereira, J. M., Coutinho, J. F., Björn, L. O., & Torres-Pereira, J. M. G. (2005). Ultraviolet-B radiation and nitrogen affect the photosynthesis of maize: A Mediterranean field study. European Journal of Agronomy, 22, 337–347.

    Article  CAS  Google Scholar 

  • Coskun, D., Britto, D. T., Li, M., Oh, S., & Kronzucker, H. J. (2013). Capacity and plasticity of potassium channels and high-affinity transporters in roots of barley and Arabidopsis. Plant Physiology, 162, 496–511.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Courbot, M., Willems, G., Motte, P., Arvidsson, S., Roosens, N., Saumitou-Laprade, P., & Verbruggen, N. (2007). A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiology, 144, 1052–1065.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Couturier, J., Montanini, B., Martin, F., Brun, A., Blaudez, D., & Chalot, M. (2007). The expanded family of ammonium transporters in the perennial poplar plant. The New Phytologist, 174, 137–150.

    Article  CAS  PubMed  Google Scholar 

  • Cubero, B., Nakagawa, Y., Jiang, X. Y., Miura, K. J., Li, F., Raghothama, K. G., Bressan, R. A., Hasegawa, P. M., & Pardo, J. M. (2009). The phosphate transporter PHT4;6 is a determinant of salt tolerance that is localized to the Golgi apparatus of Arabidopsis. Molecular Plant, 2, 535–552.

    Article  CAS  PubMed  Google Scholar 

  • Daram, P., Brunner, S., Rausch, C., Steiner, C., Amrhein, N., & Bucher, M. (1999). Pht2;1 encodes a low-affinity phosphate transporter from Arabidopsis. Plant Cell, 11, 2153–2166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Darbani, B., Noeparvar, S., & Borg, S. (2015). Deciphering mineral homeostasis in barley seed transfer cells at transcriptional level. PloS One, 10, e0141398.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • David, L. C., Dechorgnat, J., Berquin, P., Routaboul, J. M., Debeaujon, I., Daniel-Vedele, F., & Ferrario-Méry, S. (2014). Proanthocyanidin oxidation of Arabidopsis seeds is altered in mutant of the high-affinity nitrate transporter NRT2.7. Journal of Experimental Botany, 65, 885–893.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • David-Assael, O., Berezin, I., Shoshani-Knaani, N., Saul, H., Mizrachy-Dagri, T., Chen, J. X., Brook, E., & Shaul, O. (2006). AtMHX is an auxin and ABA-regulated transporter whose expression pattern suggests a role in metal homeostasis in tissues with photosynthetic potential. Functional Plant Biology, 33, 661–672.

    Article  CAS  Google Scholar 

  • Davidian, J. C., & Kopriva, S. (2010). Regulation of sulfate uptake and assimilation—The same or not the same? Molecular Plant, 3, 314–325.

    Article  CAS  PubMed  Google Scholar 

  • De Angeli, A., Monachello, D., Ephritikhine, G., Frachisse, J. M., Thomine, S., Gambale, F., & Barbier-Brygoo, H. (2006). The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature, 442, 939–942.

    Article  PubMed  CAS  Google Scholar 

  • Dell, B., & Huang, L. B. (1997). Physiological response of plants to low boron. Plant and Soil, 193, 103–120.

    Article  CAS  Google Scholar 

  • Deng, W., Luo, K. M., Li, D. M., Zheng, X. L., Wei, X. Y., Smith, W., Thammina, C., LT, L., Li, Y., & Pei, Y. (2006). Overexpression of an Arabidopsis magnesium transport gene, AtMGT1, in Nicotiana benthamiana confers Al tolerance. Journal of Experimental Botany, 57, 4235–4243.

    Article  CAS  PubMed  Google Scholar 

  • Dodd, A. N., Kudla, J., & Sanders, D. (2010). The language of calcium signaling. Annual Review of Plant Biology, 61, 593–620.

    Article  CAS  PubMed  Google Scholar 

  • Dong, B., Rengel, Z., & Delhaize, E. (1998). Uptake and translocation of phosphate by pho2 mutant and wild-type seedlings of Arabidopsis thaliana. Planta, 205, 251–256.

    Article  CAS  PubMed  Google Scholar 

  • Drummond, R. S. M., Tutone, A., Li, Y. C., & Gardner, R. C. (2006). A putative magnesium transporter AtMRS2-11 is localized to the plant chloroplast envelope membrane system. Plant Science, 170, 78–89.

    Article  CAS  Google Scholar 

  • Dubousset, L., Abdallah, M., Desfeux, A. S., Etienne, P., Meuriot, F., Hawkesford, M. J., Gombert, J., Ségura, R., Bataillé, M. P., Rezé, S., Bonnefoy, J., Ameline, A. F., Ourry, A., Le Dily, F., & Avice, J. C. (2009). Remobilization of leaf S compounds and senescence in response to restricted sulphate supply during the vegetative stage of oilseed rape are affected by mineral N availability. Journal of Experimental Botany, 60, 3239–3253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duff, S. M. G., Plaxton, W. C., & Lefebvre, D. D. (1991). Phosphate starvation responses in plant cells: De novo synthesis and degradation of acid phosphatase. Proceedings of the National Academy of Sciences of the United States of America, 88, 9538–9542.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edmeades, D. C. (2003). The long-term effects of manures and fertilisers on soil productivity and quality: A review. Nutrient Cycling in Agroecosystems, 66, 165–180.

    Article  CAS  Google Scholar 

  • Eide, D., Broderius, M., Fett, J., & Guerinot, M. L. (1996). A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proceedings of the National Academy of Sciences of the United States of America, 93, 5624–5628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elumalai, R. P., Nagpal, P., & Reed, J. W. (2002). A mutation in the Arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion. Plant Cell, 14, 119–131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Epstein, E., Rains, D., & Elzam, O. (1963). Resolution of dual mechanisms of potassium absorption by barley roots. Proceedings of the National Academy of Sciences of the United States of America, 49, 684–692.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ericsson, T., & Kahr, M. (1995). Growth and nutrition of birch seedlings at varied relative addition rates of magnesium. Tree Physiology, 15, 85–93.

    Article  CAS  PubMed  Google Scholar 

  • Fageria, N. K., Baligar, V. C., & Clark, R. B. (2002). Micronutrients in crop production. Advances in Agronomy, 77, 185–268.

    Article  CAS  Google Scholar 

  • Fan, C., Wang, X., Hu, R., Wang, Y., **ao, C., Jiang, Y., Zhang, X., Zheng, C., & YF, F. (2013). The pattern of phosphate transporter 1 genes evolutionary divergence in Glycine max L. BMC Plant Biology, 13, 48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von der Fecht-Bartenbach, J., Bogner, M., Dynowski, M., & Ludewig, U. (2010). CLC-b-mediated NO3 −/H+ exchange across the tonoplast of Arabidopsis vacuoles. Plant & Cell Physiology, 51, 960–968.

    Article  CAS  Google Scholar 

  • Fiedor, L., Kania, A., Myśliwa-Kurdziel, B., Orzeł, L., & Stochel, G. (2008). Understanding chlorophylls: Central magnesium ion and phytyl as structural determinants. Biochimica et Biophysica Acta, 1777, 1491–1500.

    Article  CAS  PubMed  Google Scholar 

  • Fita, A., Bowen, H. C., Hayden, R. M., Nuez, F., Pico, B., & Hammond, J. P. (2012). Diversity in expression of phosphorus (P) responsive genes in Cucumis melo L. PloS One, 7, e35387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Francois, L. E. (1984). Effect of excess boron on tomato yield, fruit size, and vegetative growth. Journal of the American Societyfor Horticultural Science, 109, 322–324.

    CAS  Google Scholar 

  • Gaash, R., Elazar, M., Mizrahi, K., Avramov-Mor, M., Berezin, I., & Shaul, O. (2013). Phylogeny and a structural model of plant MHX transporters. BMC Plant Biology, 13, 75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gambale, F., & Uozumi, N. (2006). Properties of Shaker-type potassium channels in higher plants. The Journal of Membrane Biology, 210, 1–19.

    Article  CAS  PubMed  Google Scholar 

  • Ganmore-Neumann, R., & Davidov, S. (1993). Uptake and distribution of calcium in rose plantlets as affected by calcium and boron concentration in culture medium. Plant and Soil, 155, 151–154.

    Article  Google Scholar 

  • Gassmann, W., Rubio, F., & Schroeder, J. I. (1996). Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. The Plant Journal, 10, 869–882.

    Article  CAS  Google Scholar 

  • Gaymard, F., Pilot, G., Lacombe, B., Bouchez, D., Bruneau, D., Boucherez, J., Michaux-Ferrière, N., Thibaud, J. B., & Sentenac, H. (1998). Identification and disruption of a plant Shaker-like outward channel involved in K+ release into the xylem sap. Cell, 94, 647–655.

    Article  CAS  PubMed  Google Scholar 

  • Gebert, M., Meschenmoser, K., Svidova, S., Weghuber, J., Schweyen, R., Eifler, K., Lenz, H., Weyand, K., & Knoop, V. (2009). A root-expressed magnesium transporter of the MRS2/MGT gene family in Arabidopsis thaliana allows for growth in low-Mg2+ environments. Plant Cell, 21, 4018–4030.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gierth, M., & Mäser, P. (2007). Potassium transporters in plants-involvement in K+ acquisition, redistribution and homeostasis. FEBS Letters, 581, 2348–2356.

    Article  CAS  PubMed  Google Scholar 

  • Gierth, M., Mäser, P., & Schroeder, J. I. (2005). The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiology, 137, 1105–1114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gigolashvili, T., & Kopriva, S. (2014). Transporters in plant sulfur metabolism. Frontiers in Plant Science, 5, 442.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gilliham, M., Dayod, M., Hocking, B., Xu, B., Conn, S., Kaiser, B., Leigh, R., & Tyerman, S. (2011). Calcium delivery and storage in plant leaves: Exploring the link with water flow. Journal of Experimental Botany, 62, 2233–2250.

    Article  CAS  PubMed  Google Scholar 

  • Gobert, A., Isayenkov, S., Voelker, C., Czempinski, K., & Maathuis, F. J. M. (2007). The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis. Proceedings of the National Academy of Sciences of the United States of America, 104, 10726–10731.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • González-Fontes, A., Rexach, J., Navarro-Gochicoa, M. T., Herrera-Rodríguez, M. B., Beato, V. M., Maldonado, J. M., & Camacho-Cristóbal, J. J. (2008). Is boron involved solely in structural roles in vascular plants? Plant Signaling & Behavior, 3, 24–26.

    Article  Google Scholar 

  • Goussias, C., Boussac, A., & Rutherford, A. W. (2002). Photosystem II and photosynthetic oxidation of water: An overview. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 357, 1369–1420.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graham, N. S., Hammond, J. P., Lysenko, A., Mayes, S., O’Lochlainn, S., Blasco, B., Bowen, H. C., Rawlings, C. J., Rios, J. J., Welham, S., Carion, P. W., Dupuy, L. X., King, G. J., White, P. J., & Broadley, M. R. (2014). Genetical and comparative genomics of Brassica under altered Ca supply identifies Arabidopsis Ca-transporter orthologs. Plant Cell, 26, 2818–2830.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregan, J., Kolisek, M., & Schweyen, R. J. (2001). Mitochondrial Mg2þ homeostasis is critical for group II intron splicing in vivo. Genes & Development, 15, 2229–2237.

    Article  CAS  Google Scholar 

  • Grotz, N., & Guerinot, M. L. (2006). Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochimica et Biophysica Acta, 1763, 595–608.

    Article  CAS  PubMed  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 of the United States of America, 95, 7220–7224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu, R., Duan, F., An, X., Zhang, F., von Wiren, N., & Yuan, L. (2013). Characterization of AMT-mediated high-affinity ammonium uptake in roots of maize (Zea mays L.) Plant & Cell Physiology, 54, 1515–1524.

    Article  CAS  Google Scholar 

  • Gu, M., Chen, A., Sun, S., & Xu, G. (2016). Complex regulation of plant phosphate transporters and the gap between molecular mechanisms and practical application: What is missing? Molecular Plant, 9, 396–416.

    Article  CAS  PubMed  Google Scholar 

  • Guan, Q., Wu, J., Yue, X., Zhang, Y., & Zhu, J. (2013). A nuclear calcium-sensing pathway is critical for gene regulation and salt stress tolerance in Arabidopsis. PloS One, 9, e1003755.

    CAS  Google Scholar 

  • Guo, K. M., Babourina, O., & Rengel, Z. (2009). Na+/H+ antiporter activity of the SOS1 gene: Lifetime imaging analysis and electrophysiological studies on Arabidopsis seedlings. Physiologia Plantarum, 137, 155–165.

    Article  CAS  PubMed  Google Scholar 

  • Guo, W., Nazim, H., Liang, Z., & Yang, D. (2016). Magnesium deficiency in plants: An urgent problem. The Crop Journal, 4, 83–91.

    Article  Google Scholar 

  • Gupta, U. C., Jame, Y. W., Campbell, C. A., Leyshon, A. J., & Nicholaichuk, W. (1985). Boron toxicity and deficiency: A review. Canadian Journal of Soil Science, 65, 381–409.

    Article  CAS  Google Scholar 

  • Gyaneshwar, P., Kumar, G. N., Parekh, L. J., & Poole, P. S. (2002). Role of soil microorganisms in improving P nutrition of plants. Plant and Soil, 245, 83–93.

    Article  CAS  Google Scholar 

  • Hammond, J. P., Broadley, M. R., & White, J. P. (2004). Genetic responses to phosphorus deficiency. Annals of Botany, 94, 323–332.

    Article  CAS  PubMed  PubMed Central  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, 391–395.

    Article  CAS  PubMed  Google Scholar 

  • Hassler, S., Lemke, L., Jung, B., Möhlmann, T., Krüger, F., Schumacher, K., Espen, L., Martinoia, E., & Neuhaus, H. E. (2012). Lack of the Golgi phosphate transporter PHT4;6 causes strong developmental defects, constitutively activated disease resistance mechanisms and altered intracellular phosphate compartmentation in Arabidopsis. The Plant Journal, 72, 732–744.

    Article  CAS  PubMed  Google Scholar 

  • Hassler, S., Jung, B., Lemke, L., Novák, O., Strnad, M., Martinoia, E., & Neuhaus, H. E. (2016). Function of the Golgi-located phosphate transporter PHT4;6 is critical for senescence-associated processes in Arabidopsis. Journal of Experimental Botany, 67, 4671–4684.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hawkesford, M. J. (2012). Improving nutrient use efficiency in crop. In eLS. Chichester, UK: Wiley.

    Google Scholar 

  • Hawkesford, M. J. (2014). Reducing the reliance on nitrogen fertilizer for wheat production. Journal of Cereal Science, 59, 276–283.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hermans, C., & Verbruggen, N. (2005). Physiological characterization of Mg deficiency in Arabidopsis thaliana. Journal of Experimental Botany, 56, 2153–2161.

    Article  CAS  PubMed  Google Scholar 

  • Hermans, C., Vuylsteke, M., Coppens, F., Cristescu, S., Harren, F., Inzé, D., & Verbruggen, N. (2010). Systems analysis of the responses to long-term magnesium deficiency and restoration in Arabidopsis thaliana. The New Phytologist, 187, 132–144.

    Article  CAS  PubMed  Google Scholar 

  • Hirsch, R. E., Lewis, B. D., Spalding, E. P., & Sussman, M. R. (1998). A role for the AKT1 potassium channel in plant nutrition. Science, 280, 918–921.

    Article  CAS  PubMed  Google Scholar 

  • Holdaway-Clarke, T. L., & Hepler, P. K. (2003). Control of pollen tube growth: Role of ion gradients and fluxes. The New Phytologist, 159, 539–563.

    Article  CAS  Google Scholar 

  • Holley, A. K., Bakthavatchalu, V., Velez-Roman, J. M., & St. Clair, D. K. (2011). Manganese superoxide dismutase: Guardian of the powerhouse. International Journal of Molecular Sciences, 12, 7114–7162.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hosoi, S., Lino, M., & Shimazaki, K. (1988). Outward-rectifying K+ channels in stomatal guard cell protoplasts. Plant & Cell Physiology, 29, 907–911.

    CAS  Google Scholar 

  • Hosy, E., Vavasseur, A., Mouline, K., Dreyer, I., Gaymard, F., Porée, F., Boucherez, J., Lebaudy, A., Bouchez, D., Very, A. A., Simonneau, T., Thibaud, J. B., & Sentenac, H. (2003). The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proceedings of the National Academy of Sciences of the United States of America, 100, 5549–5554.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, N. C., Liu, K. H., Lo, H. J., & Tsay, Y. F. (1999). Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low affinity uptake. Plant Cell, 11, 1381–1392.

    Article  CAS  PubMed  PubMed Central  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. Plant Cell, 16, 1327–1339.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain, S., Rengel, Z., Mohammadi, S. A., Ebadi-Segherloo, A., & Maqsood, M. A. (2016). Map** QTL associated with remobilization of zinc from vegetative tissues into grains of barley (Hordeum vulgare). Plant and Soil, 399, 193–208.

    Article  CAS  Google Scholar 

  • Ihemere, U. E., Narayanan, N. N., & Sayre, R. T. (2012). Iron biofortification and homeostasis in transgenic cassava roots expressing the algal iron assimilatory gene, FEA1. Frontiers in Plant Science, 3, 171.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Irigoyen, S., Karlsson, P. M., Kuruvilla, J., Spetea, C., & Versaw, W. K. (2011). The sink specific plastidic phosphate transporter PHT4;2 influences starch accumulation and leaf size in Arabidopsis. Plant Physiology, 154, 1765–1777.

    Article  CAS  Google Scholar 

  • Ishimaru, Y., Masuda, H., Suzuki, M., Bashir, K., Takahashi, M., Nakanishi, H., Mori, S., & Nishizawa, N. K. (2007). Overexpression of the OsZIP4 zinc transporter confers disarrangement of zinc distribution in rice plants. Journal of Experimental Botany, 58, 2909–2915.

    Article  CAS  PubMed  Google Scholar 

  • Javot, H., Penmetsa, R. V., Terzaghi, N., Cook, D. R., & Harrison, M. J. (2007). A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 104, 1720–1725.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson, A. A. T., 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, e24476.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karlsson, P. M., Herdean, A., Adolfsson, L., Beebo, A., Nziengui, H., Irigoyen, S., Ünnep, R., Zsiros, O., Nagy, G., Garab, G., Aronsson, H., Versaw, W. K., & Spetea, C. (2015). The Arabidopsis thylakoid transporter PHT4;1 influences phosphate availability for ATP synthesis and plant growth. The Plant Journal, 84, 99–110.

    Article  CAS  PubMed  Google Scholar 

  • Kataoka, T., Watanabe-Takahashi, A., Hayashi, N., Ohnishi, M., Mimura, T., Buchner, P., Hawkesford, M. J., Yamaya, T., & Takahashi, H. (2004). Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell, 16, 2693–2704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kato, Y., Miwa, K., Takano, J., Wada, M., & Fujiwara, T. (2009). Highly boron deficiency-tolerant plants generated by enhanced expression of NIP5;1, a boric acid channel. Plant & Cell Physiology, 50, 58–66.

    Article  CAS  Google Scholar 

  • Kendziorek, M., Barabasz, A., Rudzka, J., Tracz, K., Mills, R. F., Williams, L. E., & Antosiewicz, D. M. (2014). Approach to engineer tomato by expression of AtHMA4 to enhance Zn in the aerial parts. Journal of Plant Physiology, 171, 1413–1422.

    Article  CAS  PubMed  Google Scholar 

  • Kiba, T., & Krapp, A. (2016). Plant nitrogen acquisition under low availability: Regulation of uptake and root architecture. Plant & Cell Physiology, 57, 707–714.

    Article  CAS  Google Scholar 

  • Kiba, T., Feria-Bourrellier, A. B., Lafouge, F., Lezhneva, L., Boutet-Mercey, S., Orsel, M., Bréhaut, V., Miller, A., Daniel-Vedele, F., Sakakibara, H., & Krapp, A. (2012). The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants. Plant Cell, 24, 245–258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, T., Punshon, A., Lanzirotti, L., Li, J. M., Alonso, J. R., Ecker, J., Kaplan, M. L., & Guerinot, M. L. (2006). Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science, 314, 1295–1298.

    Article  CAS  PubMed  Google Scholar 

  • Knight, H. (1999). Calcium signaling during abiotic stress in plants. International Review of Cytology, 195, 269–324.

    Article  Google Scholar 

  • Kobayashi, T., Itai, R. N., Aung, M. S., Senoura, T., Nakanishi, H., & Nishizawa, N. K. (2012). The rice transcription factor IDEF1 directly binds to iron and other divalent metals for sensing cellular iron status. The Plant Journal, 69, 81–91.

    Article  CAS  PubMed  Google Scholar 

  • Kochian, L. V., Piñeros, M., Liu, J., & Magalhaes, J. V. (2015). Plant adaptation to acid soils: The molecular basis for crop aluminum resistance. Annual Review of Plant Biology, 66, 571–598.

    Article  CAS  PubMed  Google Scholar 

  • Kolisek, M., Zsurka, G., Samaj, J., Weghuber, J., Schweyen, R. J., & Schweigel, M. (2003). Mrs2p is an essential component of the major electrophoretic Mg2þ influx system in mitochondria. The EMBO Journal, 22, 1235–1244.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kopriva, S., Calderwood, A., Weckopp, S. C., & Koprivova, A. (2015). Plant sulfur and big data. Plant Science, 241, 1–10.

    Article  CAS  PubMed  Google Scholar 

  • Kouchi, H., & Kumazawa, K. (1975). Anatomical responses of root tips to boron deficiency II. Effect of boron deficiency on the cellular growth and development in root tips. Soil Science & Plant Nutrition, 21, 137–150.

    Article  CAS  Google Scholar 

  • Krapp, A., David, L. C., Chardin, C., Girin, T., Marmagne, A., Leprince, A. S., Chaillou, S., Ferrario-Méry, S., Meyer, C., & Daniel-Vedele, F. (2014). Nitrate transport and signaling in Arabidopsis. Journal of Experimental Botany, 65, 789–798.

    Article  CAS  PubMed  Google Scholar 

  • Kwak, J. M., Murata, Y., Baizabal-Aguirre, V. M., Merrill, J., Wang, M., Kemper, A., Hawke, S. D., Tallman, G., & Schroeder, J. I. (2001). Dominant negative guard cell K+ channel mutants reduce inward-rectifying K+ currents and light-induced stomatal opening in Arabidopsis. Plant Physiology, 127, 473–485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lacombe, B., Pilot, G., Michard, E., Gaymard, F., Sentenac, H., & Thibaud, J. B. (2000). A Shaker-like K+ channel with weak rectification is expressed in both source and sink phloem tissues of Arabidopsis. Plant Cell, 12, 837–851.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lagarde, D., Basset, M., Lepetit, M., Conejero, G., Gaymard, F., Astruc, S., & Grignon, C. (1996). Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. The Plant Journal, 9, 195–203.

    Article  CAS  PubMed  Google Scholar 

  • Lamport, D., & Várnai, P. (2013). Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development. The New Phytologist, 197, 58–64.

    Article  CAS  PubMed  Google Scholar 

  • Lapis-Gaza, H. R., Jost, R., & Finnegan, P. M. (2014). Arabidopsis PHOSPHATE TRANSPORTER1 genes PHT1;8 and PHT1;9 are involved in root-to-shoot translocation of orthophosphate. BMC Plant Biology, 14, 334.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larcher, W. (2003). Plants under stress. In W. Larcher (Ed.), Physiological ecology (pp. 321–448). Berlin: Springer.

    Chapter  Google Scholar 

  • Larisch, N., Kirsch, S. A., Schambony, A., Studtrucker, T., Böckmann, R. A., & Dietrich, P. (2016). The function of the two-pore channel TPC1 depends on dimerization of its carboxy-terminal helix. Cellular and Molecular Life Sciences, 73, 2565–2581.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lauter, F. R., Ninnemann, O., Bucher, M., Riesmeier, J., & Frommer, W. B. (1996). Preferential expression of an ammonium transporter and two putative nitrate transporters in root hairs of tomato. Proceedings of the National Academy of Sciences of the United States of America, 93, 8139–8144.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lebaudy, A., Véry, A. A., & Sentenac, H. (2007). K+ channel activity in plants: Genes, regulations and functions. FEBS Letters, 581, 2357–2366.

    Article  CAS  PubMed  Google Scholar 

  • Lee, R. B. (1988). Phosphate influx and extracellular phosphatase activity in barley roots and rose cells. The New Phytologist, 109, 141–148.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Leggewie, G., Willmitzer, L., & Riesmeier, J. W. (1997). Two cDNAs from potato are able to complement a phosphate uptake-deficient yeast mutant: Identification of phosphate transporters from higher plants. Plant Cell, 9, 381–392.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leigh, R. A., & Wyn Jones, R. G. (1984). A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. The New Phytologist, 97, 1–13.

    Article  CAS  Google Scholar 

  • Léran, S., Varala, K., Boyer, J. C., Chiurazzi, M., Crawford, N., Daniel-Vedele, F., David, L., Dickstein, R., Fernandez, E., Forde, B., Gassmann, W., Geiger, D., Gojon, A., Gong, J. M., Halkier, B. A., Harris, J. M., Hedrich, R., Limami, A. M., Rentsch, D., Seo, M., Tsay, Y. F., Zhang, M., Coruzzi, G., & Lacombe, B. (2014). A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends in Plant Science, 19, 5–9.

    Article  PubMed  CAS  Google Scholar 

  • Lezhneva, L., Kiba, T., Feria-Bourrellier, A. B., Lafouge, F., Boutet-Mercey, S., Zoufan, P., Sakakibara, H., Daniel-Vedele, F., & Krapp, A. (2014). The Arabidopsis nitrate transporter NRT2.5 plays a role in nitrate acquisition and remobilization in nitrogen-starved plants. The Plant Journal, 80, 230–241.

    Article  CAS  PubMed  Google Scholar 

  • Li, L., Tutone, A. F., Drummond, R. S., Gardner, R. C., & Luan, S. (2001). A novel family of magnesium transport genes in Arabidopsis. Plant Cell, 13, 2761–2775.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, J., Zhang, H., Lei, H., **, M., Yue, G., & Su, Y. (2016a). Functional identification of a GORK potassium channel from the ancient desert shrub Ammopiptanthus mongolicus (Maxim.) Cheng f. Plant Cell Reports, 35, 803–815.

    Article  CAS  PubMed  Google Scholar 

  • Li, S., Zhou, X., Zhao, Y., Li, H., Liu, Y., Zhu, L., Guo, J., Huang, Y., Yang, W., Fan, Y., Chen, J., & Chen, R. (2016b). Constitutive expression of the ZmZIP7 in Arabidopsis alters metal homeostasis and increases Fe and Zn content. Plant Physiology and Biochemistry, 106, 1–10.

    Article  CAS  PubMed  Google Scholar 

  • Liang, G., Yang, F., & Yu, D. (2010). MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. The Plant Journal, 62, 1046–1057.

    CAS  PubMed  Google Scholar 

  • Lin, C. M., Koh, S., Stacey, G., SM, Y., Lin, T. Y., & Tsay, Y. F. (2000). Cloning and functional characterization of a constitutively expressed nitrate transporter gene, OsNRT1, from rice. Plant Physiology, 122, 379–388.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin, S. H., Kuo, H. F., Canivenc, G., Lin, C. S., Lepetit, M., Hsu, P. K., et al. (2008). Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell, 20, 2514–2528.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin, W. Y., Lin, S. I., & Chiou, T. J. (2009a). Molecular regulators of phosphate homeostasis in plants. Journal of Experimental Botany, 60, 1427–1438.

    Article  CAS  PubMed  Google Scholar 

  • Lin, Y. F., Liang, H. M., Yang, S. Y., Boch, A., Clemens, S., Chen, C. C., JF, W., Huang, J. L., & Yeh, K. C. (2009b). Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. The New Phytologist, 182, 392–404.

    Article  CAS  PubMed  Google Scholar 

  • Liu, K. H., Huang, C. Y., & Tsay, Y. F. (1999). CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell, 11, 865–874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, T. Y., Huang, T. K., Yang, S. Y., Hong, Y. T., Huang, S. M., Wang, F. N., Chiang, S. F., Tsai, S. Y., WC, L., & Chiou, T. J. (2016). Identification of plant vacuolar transporters mediating phosphate storage. Nature Communications, 7, 11095.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lonnerdal, B. (2003). Genetically modified plants for improve trace element nutrition. The Journal of Nutrition, 133, 1490–1493.

    Google Scholar 

  • López-Arredondo, D. L., Leyva-González, M. A., Alatorre-Cobos, F., & Herrera-Estrella, L. (2013). Biotechnology of nutrient uptake and assimilation in plants. The International Journal of Developmental Biology, 57, 595–610.

    Article  PubMed  CAS  Google Scholar 

  • Loqué, D., Yuan, L., Kojima, S., Gojon, A., Wirth, J., Gazzarrini, S., Ishiyama, K., Takahashi, H., & von Wirén, N. (2006). Additive contribution of AMT1;1 and AMT1;3 to high-affinity ammonium uptake across the plasma membrane of nitrogen-deficient Arabidopsis roots. The Plant Journal, 48, 522–534.

    Article  PubMed  CAS  Google Scholar 

  • Lu, Y. P., Zhen, R. G., & Rea, P. A. (1997). AtPT4: A fourth member of the Arabidopsis phosphate transporter gene family (Accession no. U97546) Plant Gene Register PGR 97-082. Plant Physiology, 114, 747.

    Article  Google Scholar 

  • Ludewig, U., Neuhduser, B., & Dynowski, M. (2007). Molecular mechanisms of ammonium transport and accumulation in plants. FEBS Letters, 581, 2301–2308.

    Article  CAS  PubMed  Google Scholar 

  • Maathuis, F. J. M. (2009). Physiological functions of mineral macronutrients. Current Opinion in Plant Biology, 12, 250–258.

    Article  CAS  PubMed  Google Scholar 

  • Maathuis, F. J. M., & Sanders, D. (1994). Mechanism of high-affinity potassium uptake in roots of Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 91, 9272–9276.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marini, A. M., Vissers, S., Urrestarazu, A., & André, B. (1994). Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. The EMBO Journal, 13, 3456–3463.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marschner, P. (2012). Mineral nutrition of higher plants (3rd ed.). San Diego: Academic Press.

    Google Scholar 

  • Marten, I., Hoth, S., Deeken, R., Ache, P., Ketchum, K. A., Hoshi, T., & Hedrich, R. (1999). AKT3, a phloem-localized K+ channel, is blocked by protons. Proceedings of the National Academy of Sciences of the United States of America, 96, 7581–7586.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masclaux-Daubresse, C., Daniel-Vedele, F., Dechorgnat, J., Chardon, F., Gaufichon, L., & Suzuki, A. (2010). Nitrogen uptake, assimilation and remobilization in plants: Challenges for sustainable and productive agriculture. Annals of Botany, 105, 1141–1157.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mäser, P., Thomine, S., Schroeder, J. I., Ward, J. M., Hirschi, K., Sze, H., Talke, I. N., Amtmann, A., Maathuis, F. J., Sanders, D., Harper, J. F., Tchieu, J., Gribskov, M., Persans, M. W., Salt, D. E., Kim, S. A., & Guerinot, M. L. (2001). Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiology, 126, 1646–1667.

    Article  PubMed  PubMed Central  Google Scholar 

  • Masuda, H., Aung, M. S., & Nishizawa, N. K. (2013a). Iron biofortification of rice using different transgenic approaches. Rice, 6, 40.

    Article  PubMed  PubMed Central  Google Scholar 

  • Masuda, H., Kobayashi, T., Ishimaru, Y., Takahashi, M., Aung, M. S., Nakanishi, H., Mori, S., & Nishizawa, N. K. (2013b). Iron-biofortification in rice by the introduction of three barley genes participated in mugineic acid biosynthesis with soybean ferritin gene. Frontiers in Plant Science, 4, 132.

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller, A. J., Fan, X., Orsel, M., Smith, S. J., & Wells, D. M. (2007). Nitrate transport and signalling. Journal of Experimental Botany, 58, 2297–2306.

    Article  CAS  PubMed  Google Scholar 

  • Mills, R. F., Krijger, G. C., Baccarini, B. J., Hall, J. L., & Williams, L. E. (2003). Functional expression of AtHMA4, a P-1B-type ATPase of the Zn/Co/Cd/Pb subclass. The Plant Journal, 35, 164–176.

    Article  CAS  PubMed  Google Scholar 

  • Mills, R. F., Francini, A., Ferreira da Rocha, P. S. C., Bacarini, P. J., Aylett, M., Krijger, G. C., & Williams, L. E. (2005). The plant P-1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Letters, 579, 783–791.

    Article  CAS  PubMed  Google Scholar 

  • Misson, J., Thibaud, M. C., Bechtold, N., Raghothama, K., & Nussaume, L. (2004). Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants. Molecular Biology, 55, 727.

    Article  CAS  Google Scholar 

  • Mitra, G. N. (2015). Regulation of nutrient uptake by plants: A biochemical and molecular approach (pp. 1–195). New Delhi, India: Springer.

    Google Scholar 

  • Miwa, K., Takano, J., & Fujiwara, T. (2006). Improvement of seed yields under boron-limiting conditions through overexpression of BOR1, a boron transporter for xylem loading, in Arabidopsis thaliana. The Plant Journal, 46, 1084–1091.

    Article  CAS  PubMed  Google Scholar 

  • Miyaji, T., Kuromori, T., Takeuchi, Y., Yamaji, N., Yokosho, K., Shimazawa, A., Sugimoto, E., Omote, H., Ma, J. F., Shinozaki, K., & Moriyama, Y. (2015). AtPHT4;4 is a chloroplast-localized ascorbate transporter in Arabidopsis. Nature Communications, 6, 5928.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morgan, M. J., Lehmann, M., Schwarzlnder, M., Baxter, C. J., Sienkiewicz-Porzucek, A., Williams, T. C. R., & Finkemeier, I. (2008). Decrease in manganese superoxide dismutase leads to reduced root growth and affects tricarboxylic acid cycle flux and mitochondrial redox homeostasis. Plant Physiology, 147, 101–114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mouline, K., Véry, A. A., Gaymard, F., Boucherez, J., Pilot, G., Devic, M., Bouchez, D., Thibaud, J. B., & Sentenac, H. (2002). Pollen tube development and competitive ability are impaired by disruption of a Shaker K+ channel in Arabidopsis. Genes & Development, 16, 339–350.

    Article  CAS  Google Scholar 

  • Muchhal, U. S., Pardo, J. M., & Raghothama, K. G. (1996). Phosphate transporters from the higher plant Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 93, 10519–10523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mudge, S. R., Rae, A. L., Diatloff, E., & Smith, F. W. (2002). Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. The Plant Journal, 31, 341–353.

    Article  CAS  PubMed  Google Scholar 

  • Murphy, K., Reeves, P., & Jones, S. (2008). Relationship between yield and mineral nutrient concentrations in historical and modern spring wheat cultivars. Euphytica, 163, 381–390.

    Article  Google Scholar 

  • Nable, R. O., Banuelos, G. S., & Paull, J. G. (1997). Boron toxicity. Plant and Soil, 193, 181–198.

    Article  CAS  Google Scholar 

  • Nagarajan, V. K., Jain, A., Poling, M. D., Lewis, A. J., Raghothama, K. G., & Smith, A. P. (2011). Arabidopsis Pht1;5 mobilizes phosphate between source and sink organs and influences the interaction between phosphate homeostasis and ethylene signaling. Plant Physiology, 156, 1149–1163.

    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 

  • Nath, M., & Tuteja, N. (2016). NPKS uptake, sensing, and signaling and miRNAs in plant nutrient stress. Protoplasma, 253, 767–786.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ning, L., Sun, P., Wang, Q., Ma, D., Hu, Z., Zhang, D., Zhang, G., Cheng, H., & Yu, D. (2015). Genetic architecture of biofortification traits in soybean (Glycine max L. Merr.) revealed through association analysis and linkage map**. Euphytica, 204, 353–369.

    Article  Google Scholar 

  • Ninnemann, O., Jauniaux, J. C., & Frommer, W. B. (1994). Identification of a high affinity NH4+ transporter from plants. The EMBO Journal, 13, 3464–3471.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Noguchi, K., Yasumori, M., Imai, T., Naito, S., Matsunaga, T., Oda, H., Hayashi, H., Chino, M., & Fujiwara, T. (1997). bor1-1, an Arabidopsis thaliana mutant that requires a high level of boron. Plant Physiology, 115, 901–906.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noji, M., & Saito, K. (2007). Metabolic engineering of sulfur assimilation in plants. In R. T. Verpoorte, A. W. Alfermann, & T. S. Johnson (Eds.), Applications of plant metabolic engineering (pp. 297–309). Dordrecht, The Netherlands: Springer.

    Chapter  Google Scholar 

  • Nussaume, L., Kanno, S., Javot, H., Marin, E., Pochon, N., Ayadi, A., Nakanishi, T. M., & Thibaud, M. C. (2011). Phosphate import in plants: Focus on the PHT1 transporters. Frontiers in Plant Science, 2, 83.

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Lochlainn, S. O., Amoah, S., Graham, N. S., Alamer, K., Rios, J. J., Kurup, S., Stoute, A., Hammond, J. P., Ostergaard, L., King, G. J., White, P. J., & Broadley, M. R. (2011). High Resolution Melt (HRM) analysis is an efficient tool to genotype EMS mutants in complex crop genomes. Plant Methods, 7, 43.

    Article  CAS  Google Scholar 

  • O’Neill, M. A., Eberhard, S., Albersheim, P., & Darvill, A. G. (2001). Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science, 294, 846–849.

    Article  PubMed  Google Scholar 

  • Orsel, M., Filleur, S., Fraisier, V., & Daniel-Vedele, F. (2002). Nitrate transport in plant: Which gene and which control? Journal of Experimental Botany, 53, 825–833.

    Article  CAS  PubMed  Google Scholar 

  • Padmanaban, S., Chanroj, S., Kwak, J. M., Li, X., Ward, J. M., & Sze, H. (2007). Participation of endomembrane cation/H+ exchanger AtCHX20 in osmoregulation of guard cells. Plant Physiology, 44, 82–93.

    Article  CAS  Google Scholar 

  • Pandey, S., Zhang, W., & Assmann, S. M. (2007). Roles of ion channels and transporters in guard cell signal transduction. FEBS Letters, 581, 2325–2336.

    Article  CAS  PubMed  Google Scholar 

  • Pandey, P., Srivastava, R. K., & Dubey, R. S. (2013). Salicylic acid alleviates aluminum toxicity in rice seedlings better than magnesium and calcium by reducing aluminum uptake, suppressing oxidative damage and increasing antioxidative defense. Ecotoxicology, 22, 656–670.

    Article  CAS  PubMed  Google Scholar 

  • Park, S., Cheng, N. H., Pittman, J. K., Yoo, K. S., Park, J., Smith, R. H., & Hirschi, K. D. (2005). Increased calcium levels and prolonged shelf life in tomatoes expressing Arabidopsis H+/Ca2+ transporters. Plant Physiology, 139, 1194–1206.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parmar, S., Buchner, P., & Hawkesford, M. J. (2007). Leaf developmental stage affects sulfate depletion and specific sulfate transporter expression during sulfur deprivation and specific sulfate transporter expression during sulfur deprivation in Brassica napus L. Plant Biology, 9, 647–653.

    Article  CAS  PubMed  Google Scholar 

  • Pehlivan, N., Sun, L., Jarrett, P., Yang, X., Mishra, N., Chen, L., Kadioglu, S., Shen, G., & Zhang, H. (2016). Co-overexpressing a plasma membrane and a vacuolar membrane sodium/proton antiporter significantly improves salt tolerance in transgenic Arabidopsis plants. Plant & Cell Physiology, 57(5), 1069–1084. doi:10.1093/pcp/pcw055.

    Article  CAS  Google Scholar 

  • Pittman, J., & Hirschi, K. (2016). CAX-ing a wide net: Cation/H+ transporters in metal remediation and abiotic stress signaling. Plant Biology, 18(5), 741–749. doi:10.1111/plb.12460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Podgornik, M., & Pintar, M. (2007). Causes of nitrate leaching from agriculture land in Slovenia. Acta Agriculturae Slovenica, 89, 207–220.

    CAS  Google Scholar 

  • Poirier, Y., & Bucher, M. (2002). Phosphate transport and homeostasis in Arabidopsis. The Arabidopsis Book, 1, e0024. doi:10.1199/tab.0024.

    Article  PubMed  PubMed Central  Google Scholar 

  • Politi, Y., Batchelor, D., Zaslansky, P., Chmelka, B., Weaver, J., Sagi, I., Weiner, S., & Addadi, L. (2010). Role of magnesium ion in the stabilization of biogenic amorphous calcium carbonate: A structure−function investigation. Chemistry of Materials, 22, 161–166.

    Article  CAS  Google Scholar 

  • Poschenrieder, C., Llugany, M., & Barcelo, J. (1995). Short-term effects of pH and aluminum on mineral-nutrition in maize varieties differing in proton and aluminum tolerance. Journal of Plant Nutrition, 18, 1495–1507.

    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, 271–290.

    Article  CAS  Google Scholar 

  • Pyo, Y. J., Gierth, M., Schroeder, J. I., & Cho, M. H. (2010). High-affinity K+ transport in Arabidopsis: AtHAK5 and AKT1 are vital for seedling establishment and postgermination growth under low-potassium conditions. Plant Physiology, 153, 863–875.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramesh, S. A., Choimes, S., & Schachtman, D. P. (2004). Overexpression of an Arabidopsis zinc transporter in Hordeum vulgare increases short-term zinc uptake after zinc deprivation and seed zinc content. Plant Molecular Biology, 54, 373–385.

    Article  CAS  PubMed  Google Scholar 

  • Rausch, C., & Bucher, M. (2002). Molecular mechanisms of phosphate transport in plants. Planta, 216, 23–37.

    Article  CAS  PubMed  Google Scholar 

  • Remy, E., Cabrito, T. R., Batista, R. A., Teixeira, M. C., Sá-Correia, I., & Duque, P. (2012). The Pht1;9 and Pht1;8 transporters mediate inorganic phosphate acquisition by the Arabidopsis thaliana root during phosphorus starvation. The New Phytologist, 195, 356–371.

    Article  CAS  PubMed  Google Scholar 

  • Rengel, Z. (2001). Genotypic differences in micronutrient use efficiency in crops. Communications in Soil Science and Plant Analysis, 32, 1163–1186.

    Article  CAS  Google Scholar 

  • Rengel, Z. (2003). Heavy metals as essential nutrients. In M. N. V. Prasad & J. Hagemeyer (Eds.), Heavy metal stress in plants: Molecules to ecosystems (2nd ed., pp. 271–294). Berlin: Springer-Verlag.

    Google Scholar 

  • Rengel, Z., & Damon, P. M. (2008). Crops and genotypes differ in efficiency of potassium uptake and use. Physiologia Plantarum, 133, 624–636.

    Article  CAS  PubMed  Google Scholar 

  • Rengel, Z., & Marschner, P. (2005). Nutrient availability and management in the rhizosphere: Exploiting genotypic differences. The New Phytologist, 168, 305–312.

    Article  CAS  PubMed  Google Scholar 

  • Rengel, Z., Bose, J., Chen, Q., & Tripathi, B. N. (2015). Magnesium alleviates plant toxicity of aluminium and heavy metals. Crop & Pasture Science, 66, 1298–1307.

    Article  CAS  Google Scholar 

  • Ricachenevsky, F. K., Menguer, P. K., Sperotto, R. A., & Fett, J. P. (2015). Got to hide your Zn away: Molecular control of Zn accumulation and biotechnological applications. Plant Science, 236, 1–17.

    Article  CAS  PubMed  Google Scholar 

  • Richardson, A. E., Barea, J. M., McNeill, A. M., & Prigent-Combaret, C. (2009). Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant and Soil, 321, 305–339.

    Article  CAS  Google Scholar 

  • Rigas, S., Debrosses, G., Haralampidis, K., Vicente-Agullo, F., Feldmann, K. A., Grabov, A., Dolan, L., & Hatzopoulos, P. (2001). TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell, 13, 139–151.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riquelme, A., Wellmann, E., & Pinto, M. (2007). Effects of ultraviolet-B radiation on common bean (Phaseolus vulgaris L.) plants grown under nitrogen deficiency. Environmental and Experimental Botany, 60, 360–367.

    Article  CAS  Google Scholar 

  • Rosanoff, A., Weaver, C., & Rude, R. (2013). Suboptimal magnesium status in the United States: Are the health consequences underestimated? Nutrition Reviews, 70, 153–164.

    Article  Google Scholar 

  • Rouached, H., Wirtz, M., Alary, R., Hell, R., Arpat, A. B., Davidian, J. C., Fourcroy, P., & Berthomieu, P. (2008). Differential regulation of the expression of two high-affinity sulfate transporters, SULTR1.1 and SULTR1.2, in Arabidopsis. Plant Physiology, 147, 897–911.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rouached, H., Secco, D., Arpat, B., & Poirier, Y. (2011). The transcription factor PHR1 plays a key role in the regulation of sulfate shoot-to-root flux upon phosphate starvation in Arabidopsis. BMC Plant Biology, 11, 19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rout, G. R., & Sahoo, S. (2015). Role of iron in plant growth and metabolism. Reviews in Agricultural Science, 3, 1–24.

    Article  Google Scholar 

  • Rubio, F., Gassmann, W., & Schroeder, J. I. (1995). Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science, 270, 1660–1663.

    Article  CAS  PubMed  Google Scholar 

  • Ruiter, H. J. (1969). Suspected copper deficiency in radiata pine. Plant and Soil, 31, 197–200.

    Article  Google Scholar 

  • Saha, S., Mandal, B., Hazra, G. C., Dey, A., Chakraborty, M., Adhikari, B., Mukhopadhyay, S. K., & Sadhukhan, R. (2015). Can agronomic biofortification of zinc be benign for iron in cereals? Journal of Cereal Science, 65, 186–191.

    Article  CAS  Google Scholar 

  • Schmidt, W. (2006). Iron stress responses in roots of strategy I plants, chapter 11. In L. L. Barton & J. Abadia (Eds.), Iron nutrition in plants and rhizospheric microorganisms (pp. 1–435). Dordrecht, Netherlands: Springer.

    Google Scholar 

  • Schock, I., Gregan, J., Steinhauser, S., Schweyen, R., Brennicke, A., & Knoop, V. (2000). A member of a novel Arabidopsis thaliana gene family of candidate Mg2+ ion transporters complements a yeast mitochondrial group II intron-splicing mutant. The Plant Journal, 24, 489–501.

    Article  CAS  PubMed  Google Scholar 

  • Schon, M. K., & Blevins, D. G. (1990). Foliar boron applications increase the final number of branches and pods on branches of field-grown soybeans. Plant Physiology, 92, 602–607.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schroeder, J. I., Hedrich, R., & Fernandez, J. M. (1984). Potassium-selective single channels in guard cell protoplasts of Vicia faba. Nature, 312, 361–362.

    Article  CAS  Google Scholar 

  • Secco, D., Jabnoune, M., Walker, H., Shou, H., Wu, P., Poirier, Y., & Whelan, J. (2013). Spatio-temporal transcript profiling of rice roots and shoots in response to phosphate starvation and recovery. Plant Cell, 25, 4285–4304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Segonzac, C., Boyer, J. C., Ipotesi, E., Szponarski, W., Tillard, P., Touraine, B., Sommerer, N., Rossignol, M., & Gibrat, R. (2007). Nitrate efflux at the root plasma membrane: Identification of an Arabidopsis excretion transporter. Plant Cell, 19, 3760–3777.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shams, M., Etemadi, N., Baninasab, B., Ramin, A. A., & Khoshgoftarmanesh, A. H. (2010). Effect of boron and calcium on growth and quality of ‘easy lover’ cut rose. Journal of Plant Nutrition, 35, 1303–1313.

    Article  CAS  Google Scholar 

  • Shaul, O., Hilgemann, D., de-Almeida-Engler, J., Van Montagu, M., Inze, D., & Galili, G. (1999). Cloning and characterization of a novel Mg2+/H+ exchanger. The EMBO Journal, 18, 3973–3980.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen, J., Yuan, L., Zhang, J., Li, H., Bai, Z., Chen, X., Zhang, W., & Zhang, F. (2011). Phosphorus dynamics: From soil to plant. Plant Physiology, 156, 997–1005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shin, H., Shin, H. S., Dewbre, G. R., & Harrison, M. J. (2004). Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. The Plant Journal, 39, 629–642.

    Article  CAS  PubMed  Google Scholar 

  • Shukla, R., Sharma, Y. K., & Shukla, A. K. (2014). Molecular mechanism of nutrient uptake in plant. International Journal of Current Research and Academic Review, 2, 142–154.

    CAS  Google Scholar 

  • Siemianowski, O., Mills, R. F., Williams, L. E., & Antosiewicz, D. M. (2011). Expression of the P1B-type ATPase AtHMA4 in tobacco modifies Zn and Cd root to shoot partitioning and metal tolerance. Plant Biotechnology Journal, 9, 64–74.

    Article  CAS  PubMed  Google Scholar 

  • Singh, S., Korripally, P., Vancheeswaran, R., & Eapen, S. (2011). Transgenic Nicotiana tabacum plants expressing a fungal copper transporter gene show enhanced acquisition of copper. Plant Cell Reports, 30, 1929–1938.

    Article  CAS  PubMed  Google Scholar 

  • Sirichandra, C., Wasilewska, A., Vlad, F., Valon, C., & Leung, J. (2009). The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. Journal of Experimental Botany, 60, 1439–1463.

    Article  CAS  PubMed  Google Scholar 

  • Slamet-Loedin, I. H., Johnson-Beebout, S. E., Impa, S., & Tsakirpalogloul, N. (2015). Enriching rice with Zn and Fe while minimizing Cd risk. Frontiers in Plant Science, 6, 121.

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith, F. W., Ealing, P. M., Dong, B., & Delhaize, E. (1997). The cloning of two Arabidopsis genes belonging to a phosphate transporter family. The Plant Journal, 11, 83–92.

    Article  CAS  PubMed  Google Scholar 

  • Smyth, D. A., & Chevalier, P. (1984). Increases in phosphatase and b-glucosidase activities in wheat seedlings in response to phosphorus-deficient growth. Journal of Plant Nutrition, 7, 1221–1231.

    Article  CAS  Google Scholar 

  • Song, C. P., Guo, Y., Qiu, Q., Lambert, G., Galbraith, D. W., Jagendorf, A., & Zhu, J. K. (2004). A probable Na+(K+)/H+ exchanger on the chloroplast envelope functions in pH homeostasis and chloroplast development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 101, 10211–10216.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sonoda, Y., Ikeda, A., Yamaya, T., & Yamaguchi, J. (2004). Feedback regulation of the ammonium transporter gene family AMT1 by glutamine in rice. Plant & Cell Physiology, 45, S98–S98.

    Google Scholar 

  • Sreedhara, A., & Cowan, J. (2002). Structural and catalytic roles for divalent magnesium in nucleic acid biochemistry. Biometals, 15, 211–223.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi, H., Watanabe-Takahashi, A., Smith, F. W., Blake-Kalff, M., Hawkesford, M. J., & Saito, K. (2000). The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. The Plant Journal, 23, 171–182.

    Article  CAS  PubMed  Google Scholar 

  • Takano, J., Noguchi, K., Yasumori, M., Kobayashi, M., Gajdos, Z., Miwa, K., Hayashi, H., Yoneyama, T., & Fujiwara, T. (2002). Arabidopsis boron transporter for xylem loading. Nature, 420, 337–340.

    Article  CAS  PubMed  Google Scholar 

  • Takano, J., Wada, M., Ludewig, U., Schaaf, G., von Wirén, N., & Fujiwara, T. (2006). The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell, 18, 1498–1509.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tan, S., Han, R., Li, P., Yang, G., Li, S., Zhang, P., Wang, W. B., Zhao, W. Z., & Yin, L. P. (2015). Overexpression of the MxIRT1 gene increases iron and zinc content in rice seeds. Transgenic Research, 24, 109–122.

    Article  CAS  PubMed  Google Scholar 

  • Tognetti, V. B., Zurbriggen, M. D., Morandi, E. N., Fillat, M. F., Valle, E. M., Hajirezaei, M. R., & Carrillo, N. (2007). Enhanced plant tolerance to iron starvation by functional substitution of chloroplast ferredoxin with a bacterial flavodoxin. Proceedings of the National Academy of Sciences of the United States of America, 104, 11495–11500.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsay, Y. F., Schroeder, J. I., Feldmann, K. A., & Crawford, N. M. (1993). The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell, 72, 705–713.

    Article  CAS  PubMed  Google Scholar 

  • Uraguchi, S., Kato, Y., Hanaoka, H., Miwa, K., & Fujiwara, T. (2014). Generation of boron-deficiency-tolerant tomato by overexpressing an Arabidopsis thaliana borate transporter AtBOR1. Frontiers in Plant Science, 5, 125.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vance, C. P., Uhde-Stone, C., & Allan, D. (2003). Phosphorus acquisition and use: Critical adaptation by plants for securing non-renewable resources. The New Phytologist, 15, 423–447.

    Article  Google Scholar 

  • Velu, G., Ortiz-Monasterio, I., Cakmak, I., Hao, Y., & Singh, R. P. (2014). Biofortification strategies to increase grain zinc and iron concentrations in wheat. Journal of Cereal Science, 59, 365–372.

    Article  CAS  Google Scholar 

  • Verret, F., Gravot, A., Auroy, P., Preveral, S., Forestier, C., Vavasseur, A., & Richaud, P. (2004). Overexpression of AtHMA4 enhances root-to-shoot translocation od zinc and cadmium and plant metal tolerance. FEBS Letters, 576, 306–312.

    Article  CAS  PubMed  Google Scholar 

  • Versaw, W. K., & Harrison, M. J. (2002). A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell, 14, 1751–1766.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vert, G., Grotz, N., Dedaldechamp, 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. Plant Cell, 14, 1223–1233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Véry, A. A., & Sentenac, H. (2003). Molecular mechanisms and regulation of K+ transport in higher plants. Annual Review of Plant Biology, 54, 575–603.

    Article  PubMed  Google Scholar 

  • Wang, Y. Y., & Tsay, Y. F. (2011). Arabidopsis nitrate transporter NRT1.9 is important in phloem nitrate transport. Plant Cell, 23, 1945–1957.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Y., & Wu, W. H. (2015). Genetic approaches for improvement of the crop potassium acquisition and utilization efficiency. Current Opinion in Plant Biology, 25, 46–52.

    Article  PubMed  CAS  Google Scholar 

  • Wang, R., Liu, D., & Crawford, N. M. (1998). The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proceedings of the National Academy of Sciences of the United States of America, 95, 15134–15139.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Y., Ribot, C., Rezzonico, E., & Poirier, Y. (2004). Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiology, 135, 400–411.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, G. Y., Shi, J. L., Ng, G., Battle, S. L., Zhang, C., & Lu, H. (2011). Circadian clock-regulated phosphate transporter PHT4;1 plays an important role in Arabidopsis defense. Molecular Plant, 4, 516–526.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, W. H., Chen, J., Liu, T. W., Chen, J., Han, A. D., Simon, M., Dong, X. J., He, J. X., & Zheng, H. L. (2014). Regulation of the calcium-sensing receptor in both stomatal movement and photosynthetic electron transport is crucial for water use efficiency and drought tolerance in Arabidopsis. Journal of Experimental Botany, 65, 223–234.

    Article  CAS  PubMed  Google Scholar 

  • Wang, C., Yue, W., Ying, Y., Wang, S., Secco, D., Liu, Y., Whelan, J., Tyerman, S. D., & Shou, H. (2015). Rice SPX-Major Facility Super family 3, a vacuolar phosphate efflux transporter, is involved in maintaining phosphate homeostasis in rice. Plant Physiology, 169, 2822–2831.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ward, J. M., Mäser, P., & Schroeder, J. I. (2009). Plant ion channels: Gene families, physiology, and functional genomics analyses. Annual Review of Physiology, 71, 59–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waters, B., & Grusak, M. (2008). Quantitative trait locus map** for seed mineral concentrations in two Arabidopsis thaliana recombinant inbred populations. The New Phytologist, 179, 1033–1047.

    Article  CAS  PubMed  Google Scholar 

  • Wegner, L. H., & Raschke, K. (1994). Ion channels in the xylem parenchyma of barley roots. Plant Physiology, 105, 799–813.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weng, H., Yoo, C., Gosney, M., Hasegawa, P., & Mickelbart, M. (2012). Poplar GTL1 is a Ca2+/calmodulin-binding transcription factor that functions in plant water use efficiency and drought tolerance. PloS One, 7, e32925.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White, P. J., & Broadley, M. R. (2003). Calcium in plants. Annals of Botany, 92, 487–511.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams, L., & Miller, A. (2001). Transporters responsible for the uptake and partitioning of nitrogenous solutes. Annual Review of Plant Physiology and Plant Molecular Biology, 52, 659–688.

    Article  CAS  PubMed  Google Scholar 

  • Wintz, H., Fox, T., YY, W., 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. The Journal of Biological Chemistry, 278, 47644–47653.

    Article  CAS  PubMed  Google Scholar 

  • **ong, H., Guo, X., Kobayashi, T., Kakei, Y., Nakanishi, H., Nozoye, T., Zhang, L., Shen, H., Qiu, W., Nishizawa, N. K., & Zuo, Y. (2014). Expression of peanut iron regulated transporter 1 in tobacco and rice plants confers improved iron nutrition. Plant Physiology and Biochemistry, 80, 83–89.

    Article  CAS  PubMed  Google Scholar 

  • Yang, T. J., Perry, P. J., Ciani, S., Pandian, S., & Schmidt, W. (2008). Manganese deficiency alters the patterning and development of root hairs in Arabidopsis. Journal of Experimental Botany, 59, 3453–3464.

    Article  CAS  PubMed  Google Scholar 

  • Yang, S. Y., Grønlund, M., Jakobsen, I., Grotemeyer, M. S., Rentsch, D., Miyao, A., Hirochika, H., Kumar, C. S., Sundaresan, V., Salamin, N., Catausan, S., Mattes, N., Heuer, S., & Paszkowski, U. (2012). Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family. Plant Cell, 24, 4236–4251.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao, Y. A., Sun, H. Y., FS, X., Zhang, X. J., & Liu, S. Y. (2011). Comparative proteome analysis of metabolic changes by low phosphorus stress in two Brassica napus genotypes. Planta, 233, 523–537.

    Article  CAS  PubMed  Google Scholar 

  • Yi, K., Wu, Z., Zhou, J., Du, L., Guo, L., Wu, Y., & Wu, P. (2005). OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiology, 138, 2087–2096.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokosho, K., Yamaji, N., Ueno, D., Mitani, N., & Ma, J. F. (2009). OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiology, 149, 297–305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan, L., Loqué, D., Kojima, S., Rauch, S., Ishiyama, K., Inoue, E., Takahashi, H., & von Wirén, N. (2007). The organization of high-affinity ammonium uptake in Arabidopsis roots depends on the spatial arrangement and biochemical properties of AMT1-type transporters. Plant Cell, 19, 2636–2652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan, N., Yuan, S., Li, Z., Li, D., & Hu Q Luo, H. (2016). Heterologous expression of a rice miR395 gene in Nicotiana tabacum impairs sulfate homeostasis. Scientific Reports, 6, 28791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, J., Liu, B., Li, M., Feng, D., **, H., Wang, P., Liu, J., **ong, F., Wang, J., & Wang, H. B. (2015). The bHLH transcription factor bHLH104 interacts with IAA-LEUCINE RESISTANT3 and modulates iron homeostasis in Arabidopsis. Plant Cell, 27, 787–805.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, L., Versaw, W. K., Liu, J., & Harrison, M. J. (2003). A phosphate transporter from Medicago truncatula is expressed in the photosynthetic tissues of the plant and located in the chloroplast envelope. The New Phytologist, 157, 291–302.

    Article  CAS  Google Scholar 

  • Zhao, J., Cheng, N. H., Motes, C. M., Blancaflor, E. B., Moore, M., Gonzales, N., Padmanaban, S., Sze, H., Ward, J. M., & Hirschi, K. D. (2008). AtCHX13 is a plasma membrane K+ transporter. Plant Physiology, 148, 796–807.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, H., Zhou, Q., Zhou, M., Li, C., Gong, X., Liu, C., Qu, C., Wang, L., Si, W., & Hong, F. (2012). Magnesium deficiency results in damage of nitrogen and carbon cross-talk of maize and improvement by cerium addition. Biological Trace Element Research, 148, 102–109.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, Q., Ren, Y. R., Wang, Q. J., Yao, Y. X., You, C. X., & Hao, Y. J. (2016). Overexpression of MdbHLH104 gene enhances the tolerance to iron deficiency in apple. Plant Biotechnology Journal, 14(7), 1633–1645. doi:10.1111/pbi.12526.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, W., Miao, Q., Sun, D., Guodong, Y., Wu, C., Huang, J., & Zheng, C. (2012). The mitochondrial phosphate transporters modulate plant responses to salt stress via affecting ATP and gibberellin metabolism in Arabidopsis thaliana. PloS One, 7, e43530.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zuber, H., Aubert, G., Davidian, J. C., Thompson, R., & Gallardo, K. (2009). Sulfur metabolism and transport in develo** seeds. In A. Sirko, L. J. De Kok, S. Haneklaus, M. J. Hawkesford, H. Rennenberg, K. Saito, E. Schnug, & I. Stulen (Eds.), Sulfur metabolism in plants (pp. 113–118). Leiden: Backhuys Publishers.

    Google Scholar 

  • Zuber, H., Davidian, J. C., Aubert, G., Aimé, D., Belghazi, M., Lugan, R., Heintz, D., Wirtz, M., Hell, R., Thompson, R., & Gallardo, K. (2010). The seed composition of Arabidopsis mutants for the group 3 sulfate transporters indicates a role in sulfate translocation within develo** seeds. Plant Physiology, 154, 913–926.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Núcleo de Investigación en Producción Alimentaria (NIPA-UCT), Escuela de Agronomía, Facultad de Recursos Naturales, Universidad Católica de Temuco, P.O. Box 56-D, Temuco, Chile

    Claudio Inostroza-Blancheteau

  2. Laboratorio de Bioingeniería, Facultad de Ingeniería y Ciencias, Universidad Adolfo Ibáñez, Santiago, Chile

    Felipe Aquea & Felipe Moraga

  3. Laboratorio de Biología Molecular y Bioquímica, Departamento de Biología, Universidad de La Serena, P.O. Box 554, La Serena, Chile

    Cristian Ibañez

  4. Soil Science and Plant Nutrition, School of Earth and Environment, The University of Western Australia, Crawley, WA, 6009, Australia

    Zed Rengel

  5. Departamento de Ciencias Químicas y Recursos Naturales, Facultad de Ingeniería y Ciencias, Universidad de La Frontera, P.O. Box 54-D, Temuco, Chile

    Marjorie Reyes-Díaz

  6. Center of Plant, Soil Interaction and Natural Resources Biotechnology, Scientific and Technological Bioresource Nucleus (BIOREN), Universidad de La Frontera, Temuco, Chile

    Marjorie Reyes-Díaz

Authors
  1. Claudio Inostroza-Blancheteau
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  2. Felipe Aquea
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  3. Felipe Moraga
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  4. Cristian Ibañez
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  5. Zed Rengel
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  6. Marjorie Reyes-Díaz
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Corresponding author

Correspondence to Claudio Inostroza-Blancheteau .

Editor information

Editors and Affiliations

  1. Department of Botany Plant Physiology Section, Aligarh Muslim University, Aligarh, India

    M. Naeem

  2. Department of Biology Faculty of Science, University of Tabuk, Tabuk, Saudi Arabia

    Abid A. Ansari

  3. Centre for Biotechnology, Maharshi Dayanand University, Rohtak, Haryana, India

    Sarvajeet Singh Gill

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Inostroza-Blancheteau, C., Aquea, F., Moraga, F., Ibañez, C., Rengel, Z., Reyes-Díaz, M. (2017). Genetic Engineering and Molecular Strategies for Nutrient Manipulation in Plants. In: Naeem, M., Ansari, A., Gill, S. (eds) Essential Plant Nutrients. Springer, Cham. https://doi.org/10.1007/978-3-319-58841-4_17

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