Abstract
The CDF family is a ubiquitous family that has been identified in prokaryotes, eukaryotes, and archaea. Members of this family are important heavy metal transporters that transport metal ions out of the cytoplasm. In this research, a full length cDNA named Oryza sativa Zn Transporter 1 (OZT1) that closely related to rat ZnT-2 (Zn Transporter 2) gene was isolated from rice. The OZT1 encoding a CDF family protein shares 28.2 % ~ 84.3 % of identities and 49.3 % ~ 90.9 % of similarities with other zinc transporters such as RnZnT-2, HsZnT-8, RnZnT-8 and AtMTP1. OZT1 was constitutively expressed in various rice tissues. The OZT1 expression was significantly induced both in the seedlings of japonica rice Nipponbare and indica rice IR26 in response to Zn2+ and Cd2+ treatments. Besides, OZT1 expression was also increased when exposed to other excess metals, such as Cu2+, Fe2+ and Mg2+. Subcellular localization analysis indicated that OZT1 localized to vacuole. Heterologous expression of OZT1 in yeast increased tolerance to Zn2+ and Cd2+ stress but not the Mg2+ stress. Together, OZT1 is a CDF family vacuolar zinc transporter conferring tolerance to Zn2+ and Cd2+ stress, which is important to transporting and homeostasis of Zn, Cd or other heavy metals in plants.
Similar content being viewed by others
Abbreviations
- ABC:
-
ATP binding cassette
- CDF:
-
Cation diffusion facilitator
- OZT:
-
Oryza sativa zinc transporter protein
- Nramp:
-
Natural resistance-associated macrophage protein
- ZIP:
-
ZRT, IRT-like protein
- TM:
-
Transmembrane domain
- LZM:
-
Leu zipper motif
References
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 8:107. doi:10.1186/1471-2164-8-107
Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54(393):2601–2613. doi:10.1093/jxb/erg303
Kambe T, Yamaguchi-Iwai Y, Sasaki R, Nagao M (2004) Overview of mammalian zinc transporters. Cell Mol Life Sci 61(1):49–68. doi:10.1007/s00018-003-3148-y
Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol 14(2):186–199
Nies DH (1992) Czcr and Czcd, Gene-products affecting regulation of resistance to cobalt, zinc, and cadmium (Czc System) in Alcaligenes-Eutrophus. J Bacteriol 174(24):8102–8110
Paulsen IT, Saier MH (1997) A novel family of ubiquitous heavy metal ion transport proteins. J Membr Biol 156(2):99–103
Kamizono A, Nishizawa M, Teranishi Y, Murata K, Kimura A (1989) Identification of a gene conferring resistance to zinc and cadmium ions in the yeast Saccharomyces-Cerevisiae. Mol Gen Genet 219(1–2):161–167
Gustin JL, Zanis MJ, Salt DE (2011) Structure and evolution of the plant cation diffusion facilitator family of ion transporters. BMC Evol Biol 11:76. doi:10.1186/1471-2148-11-76
Podar D, Scherer J, Noordally Z, Herzyk P, Nies D, Sanders D (2011) Metal selectivity determinants in a family of transition metal transporters. J Biol Chem. doi:10.1074/jbc.M111.305649
Vallee BL, Auld DS (1990) Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29(24):5647–5659
Caulfield LE, de Onis M, Blossner M, Black RE (2004) Undernutrition as an underlying cause of child deaths associated with diarrhea, pneumonia, malaria, and measles. Am J Clin Nutr 80(1):193–198
Grotz N, Guerinot ML (2006) Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochim Biophys Acta 1763(7):595–608. doi:10.1016/j.bbamcr.2006.05.014
Welch RM, Graham RD (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55(396):353–364. doi:10.1093/jxb/erh064
Palmiter RD, Cole TB, Findley SD (1996) ZnT-2, a mammalian protein that confers resistance to zinc by facilitating vesicular sequestration. EMBO J 15(8):1784
Palmiter RD, Findley SD (1995) Cloning and functional-characterization of a mammalian zinc transporter that confers resistance to zinc. EMBO J 14(4):639–649
Zhou GA, Jiang Y, Yang Q, Wang JF, Huang J, Zhang HS (2006) Isolation and characterization of a new Na+/H+ antiporter gene OsNHA1 from rice (Oryza sativa L.). DNA Seq 17(1):24–30. doi:10.1080/10425170500224263
van der Zaal BJ, Neuteboom LW, Pinas JE, Chardonnens AN, Schat H, Verkleij JA, Hooykaas PJ (1999) Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol 119(3):1047–1055
Gietz RD, Woods RA (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350:87–96
Gietz RD, Schiestl RH (2007) Quick and easy yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2(1):35–37. doi:10.1038/nprot.2007.14
Gaither LA, Eide DJ (2001) Eukaryotic zinc transporters and their regulation. Biometals 14(3–4):251–270
Wei Y, Fu D (2005) Selective metal binding to a membrane-embedded aspartate in the Escherichia coli metal transporter YiiP (FieF). J Biol Chem 280(40):33716–33724. doi:10.1074/jbc.M506107200
Inoki K, Mori H, Wang J, Suzuki T, Hong S, Yoshida S, Blattner SM, Ikenoue T, Ruegg MA, Hall MN, Kwiatkowski DJ, Rastaldi MP, Huber TB, Kretzler M, Holzman LB, Wiggins RC, Guan KL (2011) mTORC1 activation in podocytes is a critical step in the development of diabetic nephropathy in mice. J Clin Investig 121(6):2181–2196. doi:10.1172/JCI44771
Blaudez D, Kohler A, Martin F, Sanders D, Chalot M (2003) Poplar metal tolerance protein 1 confers zinc tolerance and is an oligomeric vacuolar zinc transporter with an essential leucine zipper motif. Plant Cell 15(12):2911–2928. doi:10.1105/tpc.017541
Kobae Y, Uemura T, Sato MH, Ohnishi M, Mimura T, Nakagawa T, Maeshima M (2004) Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol 45(12):1749–1758. doi:10.1093/pcp/pci015
Desbrosses-Fonrouge AG, Voigt K, Schroder A, Arrivault S, Thomine S, Kramer U (2005) Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Lett 579(19):4165–4174. doi:10.1016/j.febslet.2005.06.046
Delhaize E (2003) Genes encoding proteins of the cation diffusion facilitator family That confer manganese tolerance. Plant Cell Online 15(5):1131–1142. doi:10.1105/tpc.009134
Drager DB, Desbrosses-Fonrouge AG, Krach C, Chardonnens AN, Meyer RC, Saumitou-Laprade P, Kramer U (2004) Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J 39(3):425–439. doi:10.1111/j.1365-313X.2004.02143.x
Persans MW, Nieman K, Salt DE (2001) Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proc Natl Acad Sci USA 98(17):9995–10000. doi:10.1073/pnas.171039798
Lang M, Hao M, Fan Q, Wang W, Mo S, Zhao W, Zhou J (2011) Functional characterization of BjCET3 and BjCET4, two new cation-efflux transporters from Brassica juncea L. J Exp Bot 62(13):4467–4480. doi:10.1093/jxb/err137
Yuan L, Yang S, Liu B, Zhang M, Wu K (2011) Molecular characterization of a rice metal tolerance protein, OsMTP1. Plant Cell Rep. doi:10.1007/s00299-011-1140-9
Delhaize E, Gruber BD, Pittman JK, White RG, Leung H, Miao Y, Jiang L, Ryan PR, Richardson AE (2007) A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. Plant J 51(2):198–210. doi:10.1111/j.1365-313X.2007.03138.x
Bloss T, Clemens S, Nies DH (2002) Characterization of the ZAT1p zinc transporter from Arabidopsis thaliana in microbial model organisms and reconstituted proteoliposomes. Planta 214(5):783–791. doi:10.1007/s00425-001-0677-1
Acknowledgments
We were indebted to David Eide providing the yeast strains DY1455 and yeast expression vector pFL61. This work was supported by National Natural Science Foundation of China (Nos. 30971556, 31071397), State Key Laboratory of Rice Biology (No. 110101) and Fundamental Research Funds for the Central Universities (No. KYZ201137).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Hong-Xia Lan and Zhou-Fei Wang contributed equally to this work.
Rights and permissions
About this article
Cite this article
Lan, HX., Wang, ZF., Wang, QH. et al. Characterization of a vacuolar zinc transporter OZT1 in rice (Oryza sativa L.). Mol Biol Rep 40, 1201–1210 (2013). https://doi.org/10.1007/s11033-012-2162-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-012-2162-2