Abstract
Zinc is an essential micronutrient for several physiological and biochemical processes. To investigate its transport in rice, we characterized OsZIP8, a rice ZIP (Zrt, Irt-like Protein) gene that is strongly up-regulated in shoots and roots under Zn deficiency. OsZIP8 could complement the growth defect of Zn-uptake yeast mutant. The OsZIP8-GFP fusion proteins were localized to the plasma membrane, suggesting that OsZIP8 is a plasma membrane zinc transporter in rice. Activation and overexpression of this gene disturbed the zinc distribution in rice plants, resulting in lower levels in shoots and mature seeds, but an increase in the roots. Field-grown transgenic plants were shorter than the WT. Under treatment with excess zinc, transgenics contained less zinc in their shoots but accumulated more in the roots. Altogether, these results demonstrate that OsZIP8 is a zinc transporter that functions in Zn uptake and distribution. Furthermore, zinc homeostasis is important to the proper growth and development of rice.
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References
An, S., Park, S., Jeong, D.H., Lee, D.Y., Kang, H.G., Yu, J.H., Hur, J., Kim, S.R., Kim, Y.H., Lee, M., et al. (2003). Generation and analysis of end sequence database for T-DNA tagging lines in rice. Plant Physiol. 133, 2040–2047.
Bughio, N., Yamaguchi, H., Nishizawa, N.K., Nakanishi, H., and Mori, S. (2002). Cloning an iron-regulated metal transporter from rice. J. Exp. Bot. 53, 1677–1682.
Cakmak, I. (2008). Enrichment of cereal grains with zinc, agronomic or genetic biofortification? Plant Soil. 302, 1–17.
Colangelo, E.P., and Guerinot, M.L. (2006). Put the metal to the petal, metal uptake and transport throughout plants. Curr. Opin. Plant Biol. 9, 322–330.
Connolly, E.L., Fett, J.P., and Guerinot, M.L. (2002). Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14, 1347–1357.
Eide, D.J. (2009). Homeostatic and adaptive responses to zinc deficiency in Saccharomyces cerevisiae. J. Biol. Chem. 284, 18565–18569.
Eide, D., Broderius, M., Fett, J., and Guerinot, M.L. (1996). A novel iron regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl. Acad. Sci. USA 93, 5624–5628.
Gaither, L.A., and Eide, D.J. (2001). Eukaryotic zinc transporters and their regulation. Biometals 14, 251–270.
Guerinot, M.L. (2000). The ZIP family of metal transporters. Biochim. Biophys. Acta 1465, 190–198.
Henriques, R., Jasik, J., Klein, M., Martinoia, E., Feller, U., Schell, J., Pais, M.S., and Koncz, C. (2002). Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Mol. Biol. 50, 587–597.
Ishimaru, Y., Suzuki, M., Kobayashi, T., Takahashi, M., Nakanishi, H., Mori, S., and Nishizawa, N.K. (2005). OsZIP4, a novel zincregulated zinc transporter in rice. J. Exp. Bot. 56, 3207–3214.
Ishimaru, Y., Suzuki, M., Tsukamoto, T., Suzuki, K., Nakazono, M., Kobayashi, T., Wada, Y., Watanabe, S., Matsuhashi, S., Takahashi, M., et al. (2006). Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J. 45, 335–346.
Ishimaru, Y., Masuda, H., Suzuki, M., Bashir, K., Takahashi, M., Nakanishi, H., Mori, S., and Nishizawa, N.K. (2007). Overexpression of the OsZIP4 zinc transporter confers disarrangement of zinc distribution in rice plants. J. Exp. Bot. 58, 2909–2915.
Jeon, J.-S., Lee, S., Jung, K.-H., Jun, S.-H., Jeong, D.H., Lee, J., Kim, C., Jang, S., Lee, S.-Y., Yang, K., et al. (2000). T-DNA insertional mutagenesis for functional genomics in rice. Plant J. 22, 561–570.
Jeong, D.H., An, S., Park, S., Kang, H.G., Park, G.G., Kim, S.R., Sim, J., Kim, Y.O., Kim, M.K., Kim, S.R., et al. (2006). Generation of a flanking sequence-tag database for activation-tagging lines in japonica rice. Plant J. 45, 123–132.
Kawachi, M., Kobae, Y., Mori, H., Tomioka, R., Lee, Y., and Maeshima, M. (2009). A mutant strain Arabidopsis thaliana that lacks vacuolar membrane zinc transporter MTP1 revealed the latent tolerance to excessive zinc. Plant Cell Physiol. 50, 1156–1170.
Kobayashi, T., Ogo, Y., Itai, R.N., Nakanishi, H., Takahashi, M., Mori, S., and Nishizawa, N.K. (2007). The transcription factor IDEF1 regulates the response to and tolerance of iron deficiency in plants. Proc. Natl. Acad. Sci. USA 104, 19150–19155.
Krämer, U., Talke, I.N., and Hanikenne, M. (2007). Transition metal transport. FEBS Lett. 581, 2263–2272.
Lee, S., and An, G. (2009). Overexpression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant Cell Environ. 32, 408–416.
Lee, S., Jeon, J.S., Jung, K.H., and An, G. (1999). Binary vector for efficient transformation of rice. J. Plant Biol. 42, 310–316.
Lee, S., Kim, Y.Y., Lee, Y., and An, G. (2007). Rice P1B-type heavymetal ATPase, OsHMA9, is a metal efflux protein. Plant Physiol. 145, 831–842.
Lin, Y.F., Liang, H.M., Yang, S.Y., Boch, A., Clemens, S., Chen, C.C., Wu, J.F., Huang, J.L., and Yeh, K.C. (2009). Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytol. 182, 392–404.
López-Millán, A.F., Ellis, D.R., and Grusak, M.A. (2004). Identification and characterization of several new members of the ZIP family of metal ion transporters in Medicago truncatula. Plant Mol. Biol. 54, 583–596.
Maser, P., Thomine, S., Schroeder, J.I., Ward, J.M., Hirschi, K., Sze, H., Talke, I.N., Amtmann, A., Maathuis, F.J., Sanders, D., et al. (2001). Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126, 1646–1667.
Mizuno, T., Usui, K., Horie, K., Nosaka, S., Mizuno, N., and Obata, H. (2005). Cloning of three ZIP/Nramp transporter genes from a Ni hyperaccumulator plant Thlaspi japonicum and their Ni2+-transport abilities. Plant Physiol. Biochem. 43, 793–801.
Moreau, S., Thomson, R.M., Kaiser, B.N., Trevaskis, B., Guerinot, M.L., Udvardi, M.K., Puppo, A., and Day, D.A. (2002). GmZIP1 encodes a symbiosis-specific zinc transporter in soybean. J. Biol. Chem. 277, 4738–4746.
Nakanishi, H., Ogawa, I., Ishimaru, Y., Mori, S., and Nishizawa, N.K. (2006). Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil. Sci. Plant Nutr. 52, 464–469.
Ogo, Y., Kobayashi, T., Itai, R.N., Nakanishi, H., Kakei, Y., Takahashi, M., Toki, S., Mori, S., and Nishizawa, N.K. (2008). A novel NAC transcription factor, IDEF2, that recognizes the iron deficiency-responsive element 2 regulates the genes involved in iron homeostasis in plants. J. Biol. Chem. 283, 13407–13417.
Palmer, C.M., and Guerinot, M.L. (2009). Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat. Chem. Biol. 5, 333–340.
Palmgren, M.G., Clemens, S., Williams, L.E., Krämer, U., Borg, S., Schjørring, J.K., and Sanders, D. (2008). Zinc biofortification of cereals, problems and solutions. Trends Plant Sci. 13, 464–473.
Park, J., Kim, Y.Y., Martinoia, E., and Lee, Y. (2008). Long-distance transporters of inorganic nutrients in plants. J. Plant Biol. 51, 240–247.
Pence, N.S., Larsen, P.B., Ebbs, S.D., Letham, D.L., Lasat, M.M., Garvin, D.F., Eide, D., and Kochian, L.V. (2000). The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc. Natl. Acad. Sci. USA 97, 4956–4960.
Ramesh, S.A., Shin, R., Eide, D.J., and Schachtman, D.P. (2003). Differential metal selectivity and gene expression of two zinc transporters from rice. Plant Physiol. 133, 126–134.
Varotto, C., Maiwald, D., Pesaresi, P., Jahns, P., Salamini, F., and Leister, D. (2002). The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant J. 31, 589–599.
Vert, G., Grotz, N., Dedaldechamp, F., Gaymard, F., Guerinot, M.L., Briat, J.F., and Curie, C. (2002). IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14, 1223–1233.
Vert, G., Barberon, M., Zelazny, E., Séguéla, M., Briat, J.F., and Curie, C. (2009). Arabidopsis IRT2 cooperates with the high-affinity iron uptake system to maintain iron homeostasis in root epidermal cells. Planta 229, 1171–1179.
Wissuwa, M., Ismail, A.M., and Yanagihara, S. (2006). Effects of zinc deficiency on rice growth and genetic factors contributing to tolerance. Plant Physiol. 142, 731–741.
Yang, X., Huang, J., Jiang, Y., and 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.). Mol. Biol. Rep. 36, 281–287.
Zhao, H., and Eide, D. (1996a). The yeast ZRT1 gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation. Proc. Natl. Acad. Sci. USA 93, 2454–2458.
Zhao, H., and Eide, D. (1996b). The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J. Biol. Chem. 271, 23203–23210.
Zhao, H., Butler, E., Rodgers, J., Spizzo, T., Duesterhoeft, S., and Eide, D. (1998). Regulation of zinc homeostasis in yeast by binding of the ZAP1 transcriptional activator to zinc-responsive promoter elements. J. Biol. Chem. 273, 28713–28720.
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Lee, S., Kim, S.A., Lee, J. et al. Zinc deficiency-inducible OsZIP8 encodes a plasma membrane-localized zinc transporter in rice. Mol Cells 29, 551–558 (2010). https://doi.org/10.1007/s10059-010-0069-0
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DOI: https://doi.org/10.1007/s10059-010-0069-0