[en] The biological processes underlying zinc homeostasis are targets for genetic improvement of crops to counter human malnutrition. Detailed phenotyping, ionomic, RNA-Seq analyses and flux measurements with (67) Zn isotope revealed whole-plant molecular events underlying zinc homeostasis upon varying zinc supply and during zinc resupply to starved Brachypodium distachyon (Brachypodium) plants. Although both zinc deficiency and excess hindered Brachypodium growth, accumulation of biomass and micronutrients into roots and shoots differed depending on zinc supply. The zinc resupply dynamics involved 1,893 zinc-responsive genes. Multiple zinc-regulated transporter and iron-regulated transporter (IRT)-like protein (ZIP) transporter genes and dozens of other genes were rapidly and transiently down-regulated in early stages of zinc resupply, suggesting a transient zinc shock, sensed locally in roots. Notably, genes with identical regulation were observed in shoots without zinc accumulation, pointing to root-to-shoot signals mediating whole-plant responses to zinc resupply. Molecular events uncovered in the grass model Brachypodium are useful for the improvement of staple monocots.
Alloway, B. J. (2008). Micronutrients and crop production: An introduction. In B. J. Alloway (Ed.), Micronutrient deficiencies in global crop production (pp. 1–39). Dordrecht: Springer Netherlands.
Anders, S., Pyl, P. T., & Huber, W. (2014). HTSeq—A python framework to work with high-throughput sequencing data. Bioinformatics, 31(2), 166–169. https://doi.org/10.1093/bioinformatics/btu638
Arsova, B., Amini, S., Scheepers, M., Baiwir, D., Mazzucchelli, G., Carnol, M., … Hanikenne, M. (2019). Resolution of the proteome, transcript and ionome dynamics upon Zn re-supply in Zn-deficient Arabidopsis. bioRxiv, 600569. https://doi.org/10.1101/600569
Assunção, A. G., Herrero, E., Lin, Y. F., Huettel, B., Talukdar, S., Smaczniak, C., … 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(22), 10296–10301.
Assunção, A. G. L., Persson, D. P., Husted, S., Schjørring, J. K., Alexander, R. D., & Aarts, M. G. M. (2013). Model of how plants sense zinc deficiency. Metallomics, 5(9), 1110–1116. https://doi.org/10.1039/C3MT00070B
Bandyopadhyay, T., Mehra, P., Hairat, S., & Giri, J. (2017). Morpho-physiological and transcriptome profiling reveal novel zinc deficiency-responsive genes in rice. Functional and Integrative Genomics, 17(5), 565–581. https://doi.org/10.1007/s10142-017-0556-x
Baxter, I., Tchieu, J., Sussman, M. R., Boutry, M., Palmgren, M. G., Gribskov, M., … Axelsen, K. B. (2003). Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiology, 132(2), 618–628.
Benedicto, A., Hernández-Apaolaza, L., Rivas, I., & Lucena, J. J. (2011). Determination of 67Zn distribution in navy bean (Phaseolus vulgaris L.) after foliar application of 67Zn-lignosulfonates using isotope pattern deconvolution. Journal of Agricultural and Food Chemistry, 59(16), 8829–8838. https://doi.org/10.1021/jf2002574
Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Brkljacic, J., Grotewold, E., Scholl, R., Mockler, T., Garvin, D. F., Vain, P., … Vogel, J. P. (2011). Brachypodium as a model for the grasses: Today and the future. Plant Physiology, 157(1), 3–13. https://doi.org/10.1104/pp.111.179531
Broadley, M. R., White, P. J., Hammond, J. P., Zelko, I., & Lux, A. (2007). Zinc in plants. The New Phytologist, 173(4), 677–702.
Castro, P. H., Lilay, G. H., Munõz-Mérida, A., Schjoerring, J. K., Azevedo, H., & Assuncąõ, A. G. L. (2017). Phylogenetic analysis of F-bZIP transcription factors indicates conservation of the zinc deficiency response across land plants. Scientific Reports, 7(1), 3806. https://doi.org/10.1038/s41598-017-03903-6
Chaney, R. L. (1993). Zinc Phytotoxicity. In A. D. Robson (Ed.), Zinc in soils and plants: Proceedings of the international symposium on ‘zinc in soils and plants’ held at the University of Western Australia, 27–28 September, 1993 (pp. 135–150). Dordrecht: Springer Netherlands.
Chen, X., & Ludewig, U. (2018). Biomass increase under zinc deficiency caused by delay of early flowering in Arabidopsis. Journal of Experimental Botany, 69(5), 1269–1279. https://doi.org/10.1093/jxb/erx478
Chen, Z., Fujii, Y., Yamaji, N., Masuda, S., Takemoto, Y., Kamiya, T., … Ueno, D. (2013). Mn tolerance in rice is mediated by MTP8. 1, a member of the cation diffusion facilitator family. Journal of Experimental Botany, 64, 4375–4387.
Chochois, V., Voge, J. P., Rebetzke, G. J., & Watt, M. (2015). Variation in adult plant phenotypes and partitioning among seed and stem-borne roots across Brachypodium distachyon accessions to exploit in breeding cereals for well-watered and drought environments. Plant Physiology, 168(3), 953–967. https://doi.org/10.1104/pp.15.00095
Choi, S., & Bird, A. J. (2014). Zinc'ing sensibly: Controlling zinc homeostasis at the transcriptional level. Metallomics, 6(7), 1198–1215. https://doi.org/10.1039/C4MT00064A
Chu, H.-H., Car, S., Socha, A. L., Hindt, M. N., Punshon, T., & Guerinot, M. L. (2017). The Arabidopsis MTP8 transporter determines the localization of manganese and iron in seeds. Scientific Reports, 7(1), 11024. https://doi.org/10.1038/s41598-017-11250-9
Claus, J., Bohmann, A., & Chavarría-Krauser, A. (2013). Zinc uptake and radial transport in roots of Arabidopsis thaliana: A modelling approach to understand accumulation. Annals of Botany, 112, 369–380. https://doi.org/10.1093/aob/mcs263
Clemens, S., Palmgren, M. G., & Kramer, U. (2002). A long way ahead: Understanding and engineering plant metal accumulation. Trends in Plant Science, 7(7), 309–315.
Colangelo, E. P., & Guerinot, M. L. (2006). Put the metal to the petal: Metal uptake and transport throughout plants. Current Opinion in Plant Biology, 9(3), 322–330.
de Abreu-Neto, J. B., Turchetto-Zolet, A. C., de Oliveira, L. F. V., Bodanese Zanettini, M. H., & Margis-Pinheiro, M. (2013). Heavy metal-associated isoprenylated plant protein (HIPP): Characterization of a family of proteins exclusive to plants. FEBS Journal, 280(7), 1604–1616. https://doi.org/10.1111/febs.12159
Durand, E., Bouchet, S., Bertin, P., Ressayre, A., Jamin, P., Charcosset, A., … Tenaillon, M. I. (2012). Flowering time in maize: Linkage and epistasis at a major effect locus. Genetics, 190(4), 1547–1562. https://doi.org/10.1534/genetics.111.136903
Evens, N. P., Buchner, P., Williams, L. E., & Hawkesford, M. J. (2017). The role of ZIP transporters and group F bZIP transcription factors in the Zn-deficiency response of wheat (Triticum aestivum). The Plant Journal, 92(2), 291–304. https://doi.org/10.1111/tpj.13655
Fukao, Y., Ferjani, A., Tomioka, R., Nagasaki, N., Kurata, R., Nishimori, Y., … Maeshima, M. (2011). iTRAQ analysis reveals mechanisms of growth defects due to excess zinc in Arabidopsis. Plant Physiology, 155(4), 1893–1907.
Glover-Cutter, K. M., Alderman, S., Dombrowski, J. E., & Martin, R. C. (2014). Enhanced oxidative stress resistance through activation of a zinc deficiency transcription factor in Brachypodium distachyon. Plant Physiology, 166(3), 1492–1505. https://doi.org/10.1104/pp.114.240457
Gupta, N., Ram, H., & Kumar, B. (2016). Mechanism of zinc absorption in plants: Uptake, transport, translocation and accumulation. Reviews in Environmental Science and Bio/Technology, 15(1), 89–109. https://doi.org/10.1007/s11157-016-9390-1
Hall, J. L., & Williams, L. E. (2003). Transition metal transporters in plants. Journal of Experimental Botany, 54(393), 2601–2613.
Hanikenne, M., Esteves, S. M., Fanara, S., & Rouached, H. (2021). An iron game: Coordinated homeostasis of essential nutrients. Journal of Experimental Botany, 72(6), 2136–2153. https://doi.org/10.1093/jxb/eraa483
Hong, S. Y., Seo, P. J., Yang, M. S., Xiang, F., & Park, C. M. (2008). Exploring valid reference genes for gene expression studies in Brachypodium distachyon by real-time PCR. BMC Plant Biology, 8(1), 1–11. https://doi.org/10.1186/1471-2229-8-112
Howe, E. A., Sinha, R., Schlauch, D., & Quackenbush, J. (2011). RNA-Seq analysis in MeV. Bioinformatics, 27(22), 3209–3210. https://doi.org/10.1093/bioinformatics/btr490
Hu, W., Coomer, T. D., Loka, D. A., Oosterhuis, D. M., & Zhou, Z. (2017). Potassium deficiency affects the carbon-nitrogen balance in cotton leaves. Plant Physiology and Biochemistry, 115, 408–417. https://doi.org/10.1016/j.plaphy.2017.04.005
Huang, S., Sasaki, A., Yamaji, N., Okada, H., Mitani-Ueno, N., & Ma, J. F. (2020). The ZIP transporter family member OsZIP9 contributes to root zinc uptake in rice under zinc-limited conditions. Plant Physiology, 183(3), 1224–1234. https://doi.org/10.1104/pp.20.00125
Hussain, D., Haydon, M. J., Wang, Y., Wong, E., Sherson, S. M., Young, J., … Cobbett, C. S. (2004). P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell, 16(5), 1327–1339.
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.
Ishimaru, Y., Suzuki, M., Ogo, Y., Takahashi, M., Nakanishi, H., Mori, S., & Nishizawa, N. K. (2008). Synthesis of nicotianamine and deoxymugineic acid is regulated by OsIRO2 in Zn excess rice plants. Soil Science and Plant Nutrition, 54(3), 417–423. https://doi.org/10.1111/j.1747-0765.2008.00259.x
Ishimaru, Y., Suzuki, M., Tsukamoto, T., Suzuki, K., Nakazono, M., Kobayashi, T., … Nishizawa, N. K. (2006). Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. The Plant Journal, 45(3), 335–346.
Jensen, J., & Pedersen, M. B. (2006). Ecological risk assessment of contaminated soil. Reviews of Environmental Contamination and Toxicology, 186, 73–105. https://doi.org/10.1007/0-387-32883-1_3
Jung, H. I., Gayomba, S. R., Yan, J., & Vatamaniuk, O. K. (2014). Brachypodium distachyon as a model system for studies of copper transport in cereal crops. Frontiers in Plant Science, 5, 236. https://doi.org/10.3389/fpls.2014.00236
Kavitha, P. G., Kuruvilla, S., & Mathew, M. K. (2015). Functional characterization of a transition metal ion transporter, OsZIP6 from rice (Oryza sativa L.). Plant Physiology and Biochemistry, 97, 165–174. https://doi.org/10.1016/j.plaphy.2015.10.005
Kim, Y. Y., Choi, H., Segami, S., Cho, H. T., Martinoia, E., Maeshima, M., & Lee, Y. (2009). AtHMA1 contributes to the detoxification of excess Zn(II) in Arabidopsis. The Plant Journal, 58, 737–753.
Klatte, M., Schuler, M., Wirtz, M., Fink-Straube, C., Hell, R., & Bauer, P. (2009). The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiology, 150(1), 257–271.
Kobayashi, T., & Nishizawa, N. K. (2012). Iron uptake, translocation, and regulation in higher plants. Annual Review of Plant Biology, 63(1), 131–152. https://doi.org/10.1146/annurev-arplant-042811-105522
Kolář, J., & Seňková, J. (2008). Reduction of mineral nutrient availability accelerates flowering of Arabidopsis thaliana. Journal of Plant Physiology, 165(15), 1601–1609. https://doi.org/10.1016/j.jplph.2007.11.010
Krämer, U. (2010). Metal hyperaccumulation in plants. Annual Review of Plant Biology, 61, 517–534.
Krämer, U., Talke, I. N., & Hanikenne, M. (2007). Transition metal transport. FEBS Letters, 581, 2263–2272.
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. https://doi.org/10.1111/j.1365-3040.2009.01935.x
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.
Lešková, A., Giehl, R. F. H., Hartmann, A., Fargašová, A., & von Wirén, N. (2017). Heavy metals induce iron deficiency responses at different hierarchic and regulatory levels. Plant Physiology, 174(3), 1648–1668. https://doi.org/10.1104/pp.16.01916
Li, S., Zhou, X., Li, H., Liu, Y., Zhu, L., Guo, J., … Chen, R. (2015). Overexpression of ZmIRT1 and ZmZIP3 enhances iron and zinc accumulation in transgenic Arabidopsis. PLoS One, 10(8), e0136647. https://doi.org/10.1371/journal.pone.0136647
Li, S., Zhou, X., Zhao, Y., Li, H., Liu, Y., Zhu, L., … Chen, R. (2016). Constitutive expression of the ZmZIP7 in Arabidopsis alters metal homeostasis and increases Fe and Zn content. Plant Physiology and Biochemistry, 106, 1–10. https://doi.org/10.1016/j.plaphy.2016.04.044
Lilay, G. H., Castro, P. H., Campilho, A., & Assunção, A. G. L. (2019). The Arabidopsis bZIP19 and bZIP23 activity requires zinc deficiency – Insight on regulation from complementation lines. Frontiers in Plant Science, 9, 1955. https://doi.org/10.3389/fpls.2018.01955
Lilay, G. H., Castro, P. H., Guedes, J. G., Almeida, D. M., Campilho, A., Azevedo, H., … Assunção, A. G. L. (2020). Rice F-bZIP transcription factors regulate the zinc deficiency response. Journal of Experimental Botany, 71(12), 3664–3677. https://doi.org/10.1093/jxb/eraa115
Lilay, G. H., Persson, D. P., Castro, P. H., Liao, F., Alexander, R. D., Aarts, M. G., & Assunção, A. G. (2021). Arabidopsis bZIP19 and bZIP23 act as zinc sensors to control plant zinc status. Nature Plants, 7(2), 137–143. https://doi.org/10.1038/s41477-021-00856-7
Liu, Z., Giehl, R. F. H., Hartmann, A., Hajirezaei, M. R., Carpentier, S., & von Wirén, N. (2020). Seminal and nodal roots of barley differ in anatomy, proteome and nitrate uptake capacity. Plant & Cell Physiology, 61(7), 1297–1308. https://doi.org/10.1093/pcp/pcaa059
Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15(12), 550. https://doi.org/10.1186/s13059-014-0550-8
MacDiarmid, C. W., Milanick, M. A., & Eide, D. J. (2003). Induction of the ZRC1 metal tolerance gene in zinc-limited yeast confers resistance to zinc shock. The Journal of Biological Chemistry, 278(17), 15065–15072.
MacFarlane, G. R., & Burchett, M. D. (2002). Toxicity, growth and accumulation relationships of copper, lead and zinc in the grey mangrove Avicennia marina (Forsk.) Vierh. Marine Environmental Research, 54(1), 65–84. https://doi.org/10.1016/S0141-1136(02)00095-8
Marschner, H., Römheld, V., & Kissel, M. (1986). Different strategies in higher plants in mobilization and uptake of iron. Journal of Plant Nutrition, 9(3–7), 695–713. https://doi.org/10.1080/01904168609363475
Martin, R. C., Vining, K., & Dombrowski, J. E. (2018). Genome-wide (ChIP-seq) identification of target genes regulated by BdbZIP10 during paraquat-induced oxidative stress. BMC Plant Biology, 18(1), 58. https://doi.org/10.1186/s12870-018-1275-8
Mendoza-Cózatl, D. G., Xie, Q., Akmakjian, G. Z., Jobe, T. O., Patel, A., Stacey, M. G., … Schroeder, J. I. (2014). OPT3 is a component of the iron-signaling network between leaves and roots and misregulation of OPT3 leads to an over-accumulation of cadmium in seeds. Molecular Plant, 7, 1455–1469. https://doi.org/10.1093/mp/ssu067
Milner, M. J., Seamon, J., Craft, E., & Kochian, L. V. (2013). Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. Journal of Experimental Botany, 64(1), 369–381. https://doi.org/10.1093/jxb/ers315
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), 1–16. https://doi.org/10.1186/1471-2164-8-107
Nagel, K. A., Kastenholz, B., Jahnke, S., van Dusschoten, D., Aach, T., Mühlich, M., … Schurr, U. (2009). Temperature responses of roots: Impact on growth, root system architecture and implications for phenotyping. Functional Plant Biology, 36(11), 947–959. https://doi.org/10.1071/FP09184
Nazri, A. Z., Griffin, J. H. C., Peaston, K. A., Alexander-Webber, D. G. A., & Williams, L. E. (2017). F-group bZIPs in barley – A role in Zn deficiency. Plant, Cell & Environment, 40, 2754–2770. https://doi.org/10.1111/pce.13045
Nouet, C., Charlier, J. B., Carnol, M., Bosman, B., Farnir, F., Motte, P., & Hanikenne, M. (2015). Functional analysis of the three HMA4 copies of the metal hyperaccumulator Arabidopsis halleri. Journal of Experimental Botany, 66(19), 5783–5795. https://doi.org/10.1093/jxb/erv280
Pertea, M., Kim, D., Pertea, G. M., Leek, J. T., & Salzberg, S. L. (2016). Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nature Protocols, 11(9), 1650–1667. https://doi.org/10.1038/nprot.2016.095
Pineau, C., Loubet, S., Lefoulon, C., Chalies, C., Fizames, C., Lacombe, B., … Richard, O. (2012). Natural variation at the FRD3 MATE transporter locus reveals cross-talk between Fe homeostasis and Zn tolerance in Arabidopsis thaliana. PLoS Genetics, 8(12), e1003120. https://doi.org/10.1371/journal.pgen.1003120
Poiré, R., Chochois, V., Sirault, X. R. R., Vogel, J. P., Watt, M., & Furbank, R. T. (2014). Digital imaging approaches for phenotyping whole plant nitrogen and phosphorus response in Brachypodium distachyon. Journal of Integrative Plant Biology, 56(8), 781–796. https://doi.org/10.1111/jipb.12198
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. https://doi.org/10.1104/pp.103.026815
Raudvere, U., Kolberg, L., Kuzmin, I., Arak, T., Adler, P., Peterson, H., & Vilo, J. (2019). G:Profiler: A web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic Acids Research, 47(W1), W191–W198. https://doi.org/10.1093/nar/gkz369
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. https://doi.org/10.1016/j.plantsci.2015.03.009
Ricachenevsky, F. K., Sperotto, R. A., Menguer, P. K., Sperb, E. R., Lopes, K. L., & Fett, J. P. (2011). ZINC-INDUCED FACILITATOR-LIKE family in plants: Lineage-specific expansion in monocotyledons and conserved genomic and expression features among rice (Oryza sativa) paralogs. BMC Plant Biology, 11(1), 20. https://doi.org/10.1186/1471-2229-11-20
Saenchai, C., Bouain, N., Kisko, M., Prom-u-thai, C., Doumas, P., & Rouached, H. (2016). The involvement of OsPHO1;1 in the regulation of iron transport through integration of phosphate and zinc deficiency signalling. Frontiers in Plant Science, 7, 396. https://doi.org/10.3389/fpls.2016.00396
Satoh-Nagasawa, N., Mori, M., Nakazawa, N., Kawamoto, T., Nagato, Y., Sakurai, K., … Akagi, H. (2012). 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. https://doi.org/10.1093/pcp/pcr166
Scheepers, M., Spielmann, J., Boulanger, M., Carnol, M., Bosman, B., De Pauw, E., … Hanikenne, M. (2020). Intertwined metal homeostasis, oxidative and biotic stress responses in the Arabidopsis frd3 mutant. The Plant Journal, 102, 34–52. https://doi.org/10.1111/tpj.14610
Schikora, A., & Schmidt, W. (2001). Iron stress-induced changes in root epidermal cell fate are regulated independently from physiological responses to low iron availability. Plant Physiology, 125(4), 1679–1687. https://doi.org/10.1104/pp.125.4.1679
Seigneurin-Berny, D., Gravot, A., Auroy, P., Mazard, C., Kraut, A., Finazzi, G., … Rolland, N. (2006). HMA1, a new cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. The Journal of Biological Chemistry, 281(5), 2882–2892.
Shabala, S., White, R. G., Djordjevic, M. A., Ruan, Y.-L., & Mathesius, U. (2016). Root-to-shoot signalling: Integration of diverse molecules, pathways and functions. Functional Plant Biology, 43(2), 87–104. https://doi.org/10.1071/FP15252
Shanmugam, V., Tsednee, M., & Yeh, K.-C. (2012). ZINC TOLERANCE INDUCED BY IRON 1 reveals the importance of glutathione in the cross-homeostasis between zinc and iron in Arabidopsis thaliana. The Plant Journal, 69(6), 1006–1017. https://doi.org/10.1111/j.1365-313X.2011.04850.x
Shin, L. J., Lo, J. C., & Yeh, K. C. (2012). Copper chaperone antioxidant Protein1 is essential for copper homeostasis. Plant Physiology, 159(3), 1099–1110. https://doi.org/10.1104/pp.112.195974
Shojima, S., Nishizawa, N. K., Fushiya, S., Nozoe, S., Irifune, T., & Mori, S. (1990). Biosynthesis of phytosiderophores: In vitro biosynthesis of 2′-deoxymugineic acid from L-methionine and nicotianamine. Plant Physiology, 93(4), 1497–1503. https://doi.org/10.1104/pp.93.4.1497
Simm, C., Lahner, B., Salt, D., LeFurgey, A., Ingram, P., Yandell, B., & Eide, D. J. (2007). Saccharomyces cerevisiae vacuole in zinc storage and intracellular zinc distribution. Eukaryotic Cell, 6(7), 1166–1177. https://doi.org/10.1128/EC.00077-07
Sinclair, S. A., & Krämer, U. (2012). The zinc homeostasis network of land plants. Biochimica et Biophysica Acta, 1823, 1553–1567. https://doi.org/10.1016/j.bbamcr.2012.05.016
Sinclair, S. A., Senger, T., Talke, I. N., Cobbett, C. S., Haydon, M. J., & Kraemer, U. (2018). Systemic upregulation of MTP2- and HMA2-mediated Zn partitioning to the shoot supplements local Zn deficiency responses of Arabidopsis. The Plant Cell, 30, 2463–2479. https://doi.org/10.1105/tpc.18.00207
Smith, D. D., Sperry, J. S., & Adler, F. R. (2017). Convergence in leaf size versus twig leaf area scaling: Do plants optimize leaf area partitioning? Annals of Botany, 119(3), 447–456.
Spielmann, J., Ahmadi, H., Scheepers, M., Weber, M., Nitsche, S., Carnol, M., … Hanikenne, M. (2020). The two copies of the zinc and cadmium ZIP6 transporter of Arabidopsis halleri have distinct effects on cadmium tolerance. Plant, Cell & Environment, 43, 2143–2157. https://doi.org/10.1111/pce.13806
Steffens, B., & Rasmussen, A. (2016). The physiology of adventitious roots. Plant Physiology, 170(2), 603–617. https://doi.org/10.1104/pp.15.01360
Subedi, S. R., Sandhu, N., Singh, V. K., Sinha, P., Kumar, S., Singh, S. P., … Kumar, A. (2019). Genome-wide association study reveals significant genomic regions for improving yield, adaptability of rice under dry direct seeded cultivation condition. BMC Genomics, 20(1), 471–471. https://doi.org/10.1186/s12864-019-5840-9
Suzuki, M., Takahashi, M., Tsukamoto, T., Watanabe, S., Matsuhashi, S., Yazaki, J., … Nishizawa, N. K. (2006). Biosynthesis and secretion of mugineic acid family phytosiderophores in zinc-deficient barley. The Plant Journal, 48(1), 85–97.
Suzuki, M., Tsukamoto, T., Inoue, H., Watanabe, S., Matsuhashi, S., Takahashi, M., … Nishizawa, N. K. (2008). Deoxymugineic acid increases Zn translocation in Zn-deficient rice plants. Plant Molecular Biology, 66(6), 609–617. https://doi.org/10.1007/s11103-008-9292-x
Takahashi, M., Yamaguchi, H., Nakanishi, H., Shioiri, T., Nishizawa, N. K., & Mori, S. (1999). Cloning two genes for nicotianamine aminotransferase, a critical enzyme in iron acquisition (strategy II) in graminaceous plants. Plant Physiology, 121(3), 947–956. https://doi.org/10.1104/pp.121.3.947
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. https://doi.org/10.1111/j.1365-3040.2012.02527.x
Takei, K., Takahashi, T., Sugiyama, T., Yamaya, T., & Sakakibara, H. (2002). Multiple routes communicating nitrogen availability from roots to shoots: A signal transduction pathway mediated by Cytokinin. Journal of Experimental Botany, 53(370), 971–977. https://doi.org/10.1093/JEXBOT/53.370.971
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.
Tennant, D. (1976). Root growth of wheat. I. Early patterns of multiplication and extension of wheat roots including effects of levels of nitrogen, phosphorus and potassium. Australian Journal of Agricultural Research, 27(2), 183–183. https://doi.org/10.1071/ar9760183
The International Brachypodium Initiative. (2010). Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature, 463(7282), 763–768. https://doi.org/10.1038/nature08747
Tiong, J., McDonald, G. K., Genc, Y., Pedas, P., Hayes, J. E., Toubia, J., … Huang, C. Y. (2014). HvZIP7 mediates zinc accumulation in barley (Hordeum vulgare) at moderately high zinc supply. New Phytologist, 201, 131–143. https://doi.org/10.1111/nph.12468
Vallee, B. L., & Falchuk, K. H. (1993). The biochemical basis of zinc physiology. Physiological Reviews, 73(1), 79–118. https://doi.org/10.1152/physrev.1993.73.1.79
Vatansever, R., Filiz, E., & Eroglu, S. (2017). Genome-wide exploration of metal tolerance protein (MTP) genes in common wheat (Triticum aestivum): Insights into metal homeostasis and biofortification. Biometals, 30, 217–235. https://doi.org/10.1007/s10534-017-9997-x
Vert, G. A., Briat, J. F., & Curie, C. (2003). Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiology, 132(2), 796–804. https://doi.org/10.1104/pp.102.016089
Von Wirén, N., Marschner, H., & Romheld, V. (1996). Roots of iron-efficient maize also absorb Phytosiderophore-chelated zinc. Plant Physiology, 111(4), 1119–1125. https://doi.org/10.1104/pp.111.4.1119
Walker, J. M., Tsivkovskii, R., & Lutsenko, S. (2002). Metallochaperone Atox1 transfers copper to the NH2-terminal domain of the Wilson's disease protein and regulates its catalytic activity. Journal of Biological Chemistry, 277(31), 27953–27959. https://doi.org/10.1074/jbc.M203845200
Wang, H. Y., Klatte, M., Jakoby, M., Baumlein, H., Weisshaar, B., & Bauer, P. (2007). Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana. Planta, 226(4), 897–908.
Watt, M., Schneebeli, K., Dong, P., & Wilson, I. W. (2009). The shoot and root growth of Brachypodium and its potential as a model for wheat and other cereal crops. Functional Plant Biology, 36(11), 960–969. https://doi.org/10.1071/FP09214
Wintz, H., Fox, T., Wu, Y. Y., Feng, V., Chen, W., Chang, H. S., … Vulpe, C. (2003). Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. The Journal of Biological Chemistry, 278(48), 47644–47653.
Yamada, K., Nagano, A. J., Nishina, M., Hara-Nishimura, I., & Nishimura, M. (2013). Identification of two novel endoplasmic reticulum body-specific integral membrane proteins. Plant Physiology, 161(1), 108–120. https://doi.org/10.1104/pp.112.207654
Yang, M., Zhang, Y., Zhang, L., Hu, J., Zhang, X., Lu, K., … Lian, X. (2014). OsNRAMP5 contributes to manganese translocation and distribution in rice shoots. Journal of Experimental Botany, 65(17), 4849–4861. https://doi.org/10.1093/jxb/eru259
Yang, X., Huang, J., Jiang, Y., & Zhang, H. S. (2009). Cloning and functional identification of two members of the ZIP (Zrt, Irt-like protein) gene family in rice (Oryza sativa L.). Molecular Biology Reports, 36(2), 281–287. https://doi.org/10.1007/s11033-007-9177-0
Yordem, B. K., Conte, S. S., Ma, J. F., Yokosho, K., Vasques, K. A., Gopalsamy, S. N., & Walker, E. L. (2011). Brachypodium distachyon as a new model system for understanding iron homeostasis in grasses: Phylogenetic and expression analysis of yellow stripe-like (YSL) transporters. Annals of Botany, 108(5), 821–833. https://doi.org/10.1093/aob/mcr200
Zargar, S. M., Kurata, R., Inaba, S., Oikawa, A., Fukui, R., Ogata, Y., … Fukao, Y. (2015). Quantitative proteomics of Arabidopsis shoot microsomal proteins reveals a cross-talk between excess zinc and iron deficiency. Proteomics, 15, 1196–1201. https://doi.org/10.1002/pmic.201400467
Zeng, H., Zhang, X., Ding, M., & Zhu, Y. (2019). Integrated analyses of miRNAome and transcriptome reveal zinc deficiency responses in rice seedlings. BMC Plant Biology, 19(1), 585. https://doi.org/10.1186/s12870-019-2203-2
Zhang, Y., Chen, K., Zhao, F. J., Sun, C., Jin, C., Shi, Y., … Lian, X. (2018). OsATX1 interacts with heavy metal P1B-type ATPases and affects copper transport and distribution. Plant Physiology, 178(1), 329–344. https://doi.org/10.1104/pp.18.00425