Skip to main content
SpringerLink
Log in

OsZIP5 is a plasma membrane zinc transporter in rice

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Zinc is essential for normal plant growth and development. To understand its transport in rice, we characterized OsZIP5, which is inducible under Zn deficiency. OsZIP5 complemented the growth defect of a yeast Zn-uptake mutant, indicating that OsZIP5 is a Zn transporter. The OsZIP5-GFP fusion protein was localized to the plasma membrane. Transgenic plants overexpressing the gene grew less well. Overexpression of the gene decreased the Zn concentration in shoots, but caused it to rise in the roots. Knockout plants showed no visible phenotypic changes under either normal or deficient conditions. However, they were tolerant to excess Zn and contained less Zn. In contrast, overexpressing transgenics were sensitive to excess Zn. These results indicate that OsZIP5 plays a role in Zn distribution within rice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • An G, Ebert PR, Mitra A, Ha SB (1988) Binary vectors. In: Gelvin SB, Schilperoort RA (eds) Plant molecular biology manual. Martinus Nijhoff Publishers, Leiden

    Google Scholar 

  • An S, Park S, Jeong DH et al (2003) Generation and analysis of end sequence database for T-DNA tagging lines in rice. Plant Physiol 133:2040–2047

    Article  CAS  PubMed  Google Scholar 

  • Bughio N, Yamaguchi H, Nishizawa NK, Nakanishi H, Mori S (2002) Cloning an iron regulated metal transporter from rice. J Exp Bot 53:1677–1682

    Article  CAS  PubMed  Google Scholar 

  • Cakmak I (2000) Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol 146:185–205

    Article  CAS  Google Scholar 

  • Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17

    Article  CAS  Google Scholar 

  • Colangelo EP, Guerinot ML (2006) Put the metal to the petal: metal uptake and transport throughout plants. Curr Opin Plant Biol 9:322–330

    Article  CAS  PubMed  Google Scholar 

  • Coleman JE (1998) Zinc enzymes. Curr Opin Chem Biol 2:222–234

    Article  CAS  PubMed  Google Scholar 

  • Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA 93:5624–5628

    Article  CAS  PubMed  Google Scholar 

  • Gietz RD, Schiestl RH (1995) Transforming yeast with DNA. Meth Mol Cell Biol 5:255–269

    Google Scholar 

  • Grandjean O, Vernoux T, Laufs P, Belcram K, Mizukami Y, Traas J (2004) In vivo analysis of cell division, cell growth, and differentiation at the shoot apical meristem in Arabidopsis. Plant Cell 16:74–87

    Article  CAS  PubMed  Google Scholar 

  • Grotz N, Guerinot ML (2006) Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochim Biophys Acta 1763:595–608

    Article  CAS  PubMed  Google Scholar 

  • Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465:190–198

    Article  CAS  PubMed  Google Scholar 

  • Han MJ, Jung KH, Yi G, Lee DY, An G (2006) Rice immature pollen 1 (RIP1) is a regulator of late pollen development. Plant Cell Physiol 47:1457–1472

    Article  CAS  PubMed  Google Scholar 

  • Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506

    Article  CAS  PubMed  Google Scholar 

  • Henriques R, Jasik J, Klein M, Martinoia E, Feller U, Schell J, Pais MS, 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

    Article  CAS  PubMed  Google Scholar 

  • Ishimaru Y, Suzuki M, Kobayashi T, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2005) OsZIP4, a novel zinc-regulated zinc transporter in rice. J Exp Bot 56:3207–3214

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ishimaru Y, Masuda H, Suzuki M, Bashir K, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2007) Overexpression of the OsZIP4 zinc transporter confers disarrangement of zinc distribution in rice plants. J Exp Bot 58:2909–2915

    Article  CAS  PubMed  Google Scholar 

  • 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, Nam J-M, An K, Han M-J, Sung R-J, Choi H-S, Yu J-W, Choi J-H, Cho S-Y, Cha S-S, An G (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22:561–570

    Article  CAS  PubMed  Google Scholar 

  • Jeong DH, An S, Park S, Kang HG, Park GG, Kim SR, Sim J, Kim YO, Kim MK, Kim SR, Kim J, Shin M, Jung M, An G (2006) Generation of a flanking sequence-tag database for activation-tagging lines in japonica rice. Plant J 45:123–132

    Article  CAS  PubMed  Google Scholar 

  • Krämer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Jeon JS, Jung KH, An G (1999) Binary vector for efficient transformation of rice. J Plant Biol 42:310–316

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lin YF, Liang HM, Yang SY, Boch A, Clemens S, Chen CC, Wu JF, Huang JL, Yeh KC (2009) Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytol 182:392–404

    Article  CAS  PubMed  Google Scholar 

  • López-Millán AF, Ellis DR, Grusak MA (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

    Article  PubMed  Google Scholar 

  • Maser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667

    Article  CAS  PubMed  Google Scholar 

  • Moreau S, Thomson RM, Kaiser BN, Trevaskis B, Guerinot ML, Udvardi MK, Puppo A, Day DA (2002) GmZIP1 encodes a symbiosis-specific zinc transporter in soybean. J Biol Chem 277:4738–4746

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Pahlsson A (1989) Toxicity of heavy metals (Zn, Cu, Cd, Pb) to vascular plants. Water Air Soil Pollut 47:287–319

    Article  Google Scholar 

  • Palmgren MG, Clemens S, Williams LE, Krämer U, Borg S, Schjørring JK, Sanders D (2008) Zinc biofortification of cereals: problems and solutions. Trends Plant Sci 13:464–473

    Article  CAS  PubMed  Google Scholar 

  • Price A, Hendry G (1991) Iron-catalysed oxygen radical formation and its possible contribution to drought damage in nine native grasses and three cereals. Plant Cell Environ 14:477–484

    Article  CAS  Google Scholar 

  • Ramesh SA, Choimes S, Schachtman DP (2004) Over-expression of an Arabidopsis zinc transporter in Hordeum vulgare increases short-term zinc uptake after zinc deprivation and seed zinc content. Plant Mol Biol 54:373–385

    Article  CAS  PubMed  Google Scholar 

  • Rentsch D, Laloi M, Rouhara I, Schmelzer E, Delrot S, Frommer WB (1995) NTR1 encodes a high-affinity oligopeptide transporter in Arabidopsis. FEBS Lett 370:264–268

    Article  CAS  PubMed  Google Scholar 

  • Rhodes D, Klug A (1993) Zinc fingers. Sci Am 268:56–65

    Article  CAS  PubMed  Google Scholar 

  • Supek F, Supekova L, Nelson H, Nelson N (1996) A yeast manganese transporter related to the macrophage protein involved in conferring resistance to mycobacteria. Proc Natl Acad Sci USA 93:5105–5110

    Article  CAS  PubMed  Google Scholar 

  • Suzuki M, Tsukamoto T, Inoue H, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2008) Deoxymugineic acid increases Zn translocation in Zn-deficient rice plants. Plant Mol Biol 66:609–617

    Article  CAS  PubMed  Google Scholar 

  • Vallee BL, Auld DS (1990) Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29:5647–5659

    Article  CAS  PubMed  Google Scholar 

  • Vallee BL, Falchuk KH (1993) The biochemical basis of zinc physiology. Physiol Rev 73:79–118

    CAS  PubMed  Google Scholar 

  • Varotto C, Maiwald D, Pesaresi P, Jahns P, Salamini F, Leister D (2002) The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant J 31:589–599

    Article  CAS  PubMed  Google Scholar 

  • Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF, 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  Google Scholar 

  • Yang X, Huang J, Jiang Y, Zhang HS (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

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, 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

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Eide D (1996b) The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J Bio Chem 271:23203–23210

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank In-Soon Park and Kyungsook An for generating the transgenic lines, Yoonja Cho for managing the transgenic seeds, and Chang-Duk Jung for growing the transformed plants. This work was supported in part by grants from the Crop Functional Genomic Center, the twentyfirst Century Frontier Program (Grant CG1111); the Biogreen 21 Program (034-001-007-03-00), Rural Development Administration; the Basic Research Promotion Fund (KRF-2007-341-C00028); Kyung Hee University; and the National Science Foundation (grant no. DB10701119 to M.L.G.).

Author information

Authors and Affiliations

  1. Department of Plant Molecular Systems Biotechnology and Crop Biotech Institute, Kyung Hee University, Yongin, 446-701, Republic of Korea

    Sichul Lee, Hee Joong Jeong & Gynheung An

  2. Integrative Biosciences and Biotechnology, Pohang University of Science and Technology (POSTECH), Pohang, 790-784, Republic of Korea

    Sichul Lee, Hee Joong Jeong & Gynheung An

  3. Department of Biological Sciences, Dartmouth College, Hanover, NH, 03755, USA

    Sichul Lee, Sun A. Kim, Joohyun Lee & Mary Lou Guerinot

Authors
  1. Sichul Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hee Joong Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sun A. Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joohyun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mary Lou Guerinot
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gynheung An
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gynheung An.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11103_2010_9637_MOESM1_ESM.tif

Supplemental Fig. S1 Phylogenic analysis of ZIP members from Arabidopsis and rice. Protein sequences were aligned using the Clustal X and phylogenetic tree was visualized with MEGA program. Accession numbers: AB070226 for OsIRT1; AB126086 for OsIRT2; AY302058 for OsZIP1; AY302059 for OsZIP2; AY323915 for OsZIP3; AB126089 for OsZIP4; AB126087 for OsZIP5; AB126088 for OsZIP6; AB126090 for OsZIP7; AY324148 for OsZIP8; LOC_Os05g39540 for OsZIP9; LOC_Os06g37010 for OsZIP10; AAC24197 for AtZIP1; AAC24198 for AtZIP2; AAC24199 for AtZIP3; AAB65480 for AtZIP4; AAL38432 for AtZIP5; AAL38433 for AtZIP6; AAL38434 for AtZIP7; AAL83293 for AtZIP8; AAL38435 for AtZIP9; AAL38436 for AtZIP10; AAL67953 for AtZIP11; AAL38437 for AtZIP12; AAB01678 for AtIRT1; NP_001031670 for AtIRT2; NP_564766 for AtIRT3. (TIFF 838 kb)

11103_2010_9637_MOESM2_ESM.tif

Supplemental Fig. S2 Roots expressing GFP under control of CaMV 35S promoter (P35S-GFP). GFP fluorescence in control was detected throughout cytosol. Fluorescence (left) and bright-field (middle) images are overlaid at right. Bars = 10 µm. (TIFF 1710 kb)

11103_2010_9637_MOESM3_ESM.tif

Supplemental Fig. S3 Cu (a) and Mn (b) contents were measured from four flag leaves at flowering stage. Error bars represent standard deviation. Significant differences from WT were determined by Student’s t test, * P < 0.05. (TIFF 43 kb)

11103_2010_9637_MOESM4_ESM.tif

Supplemental Fig. S4 Quantification of WT and OsZIP5 mutant plants grown on Fe-deficient (a), Cu-deficient (b), and Mn-deficient (c) media for 8 days following germination. Heights of WT, oszip5-1 oszip5-2, Z5OX-5, and Z5OX-6 plants (n = 8 each) are shown. (TIFF 66 kb)

11103_2010_9637_MOESM5_ESM.tif

Supplemental Fig. S5 Metal-ion measurements at seedling stage. Iron concentrations in shoots and roots from WT, oszip5-1, oszip5-2, Z5OX-5, and Z5OX-6 plants grown on Fe-sufficient (a) or -deficient (b) media (n = 4 each). Cu (c) and Mn (d) concentrations in shoots and roots grown on control MS medium (n = 4 each). (TIFF 128 kb)

11103_2010_9637_MOESM6_ESM.tif

Supplemental Fig. S6 Concentrations of Cu (a) and Mn (b) in mature seeds. Error bars represent standard deviation. Ten seeds were pooled, with four replicates prepared. Significant differences from WT were determined by Student’s t-tests.* P < 0.05. (TIFF 41 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lee, S., Jeong, H.J., Kim, S.A. et al. OsZIP5 is a plasma membrane zinc transporter in rice. Plant Mol Biol 73, 507–517 (2010). https://doi.org/10.1007/s11103-010-9637-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-010-9637-0

Keywords

Search

Navigation