Cloning and characterisation of ZmZLP1, a gene encoding an endoplasmic reticulum-localised zinc transporter in Zea mays
Yao-Guang Xu A , Bao-Sheng Wang A , Jing-Juan Yu A , Guang-Ming Ao A and Qian Zhao A BA State Key Laboratory of Agribiotechnology, China Agricultural University, Beijing 100193, China.
B Corresponding author. Email: zhaoqian@cau.edu.cn
Functional Plant Biology 37(3) 194-205 https://doi.org/10.1071/FP09045
Submitted: 24 February 2009 Accepted: 12 November 2009 Published: 25 February 2010
Abstract
The ZmZLP1 (ZmZIP-like protein) gene was isolated from a cDNA library of Zea mays L. (maize) pollen. Bioinformatics analysis indicated that ZmZLP1 shares many characteristics of the ZIP (ZRT/IRT-like protein) family of metal ion transporters. Under general nutrient conditions, the expression of ZmZLP1 was detected in both mature pollen and, less strongly, in male inflorescences, whereas an induction of the ZmZLP1 transcript was observed in roots after 12 h of zinc deprivation. The visualisation of GFP showed that ZmZLP1 was targeted to the endoplasmic reticulum (ER). To investigate the gene’s functions, we fused ZmZLP1 with the signal peptide of the plasma membrane-localised protein AtIRT1 and transformed this fusion protein into the zinc uptake-deficient yeast (Saccharomyces cerevisiae) strain ZHY3 and the wild-type strain DEY1457. The IRT1-ZmZLP1 transformants grew poorly on zinc-limited medium, and this growth defect was rescued by zinc supplementation, suggesting that ZmZLP1 is responsible for transporting zinc from the ER to the cytoplasm. Further research indicated that ZmZLP1 is involved in the unfolded protein response (UPR) pathway and enhances the heat resistance of yeast cells.
Additional keywords: corn, maize, subcellular localisation, unfolded protein response, zinc deficiency induction, ZIP family.
Acknowledgements
We thank Elixigen Corporation for critical comments on the manuscript. This work was supported by a project (no. 2008ZX08009-003) from the Ministry of Agriculture of China for transgenic research.
Assuncao AGL,
Costa Martins PDA,
De Folter S,
Vooijs R,
Schat H, Aarts MGM
(2001) Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant, Cell & Environment 24, 217–226.
| Crossref | GoogleScholarGoogle Scholar |
Burleigh SH,
Kristensen BK, Bechmann IE
(2003) A plasma membrane zinc transporter from Medicago truncatula is up-regulated in roots by Zn fertilization, yet down-regulated by arbuscular mycorrhizal colonization. Plant Molecular Biology 52, 1077–1088.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chauhan RS
(2006) Bioinformatics approach toward identification of candidate genes for zinc and iron transporters in maize. Current Science 91, 510–515.
Cohen CK,
Fox TC,
Garvin DF, Kochian LV
(1998) The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiology 116, 1063–1072.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Eckhardt U,
Mas Marques A, Buckhout TJ
(2001) Two iron-regulated cation transporters from tomato complement metal uptake-deficient yeast mutants. Plant Molecular Biology 45, 437–448.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Eide DJ
(2006) Zinc transporters and the cellular trafficking of zinc. Biochimica et Biophysica Acta 1763, 711–722.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Eide D,
Broderius M,
Fett J, Guerinot ML
(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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ellis CD,
Wang F,
MacDiarmid CW,
Clark S,
Lyons T, Eide DJ
(2004) Zinc and the Msc2 zinc transporter protein are required for endoplasmic reticulum function. The Journal of Cell Biology 166, 325–335.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ellis CD,
MacDiarmid CW, Eide DJ
(2005) Heteromeric protein complexes mediate zinc transport into the secretory pathway of eukaryotic cells. The Journal of Biological Chemistry 280, 28811–28818.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gietz D,
St. Jean A,
Wood RA, Schiestl RH
(1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Research 20, 1425.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Grotz N, Guerinot ML
(2006) Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochimica et Biophysica Acta 1763, 595–608.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Grotz N,
Fox T,
Connolly E,
Park W,
Guerinot ML, 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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Guerinot ML
(2000) The ZIP family of metal transporters. Biochimica et Biophysica Acta 1465, 190–198.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hofgen R, Willmitzer L
(1988) Storage of competent cell for Agrobacterium transformation. Nucleic Acids Research 16, 9877.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ishimaru Y,
Suzuki M,
Kobayashi T,
Takahashi M,
Nakanishi H,
Mori S, Nishizawa NK
(2005) OsZIP4, a novel zinc-regulated zinc transporter in rice. Journal of Experimental Botany 56, 3207–3214.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kambe T,
Yamaguchi-Iwai Y,
Sasaki R, Nagao M
(2004) Overview of mammalian zinc transporters. Cellular and Molecular Life Sciences 61, 49–68.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kaufman RJ
(1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes & Development 13, 1211–1233.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kumanovics A,
Poruk KE,
Osborn KA,
Ward DM, Kaplan J
(2006) YKE4 (YIL023C) Encodes a bidirectional zinc transporter in the endoplasmic reticulum of Saccharomyces cerevisiae. The Journal of Biological Chemistry 281, 22566–22574.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lasswell J,
Rogg JE,
Nelson DC,
Rongey C, Bartel B
(2000) Cloning and characterization of IAR1, a gene required for auxin conjugate sensitivity in Arabidopsis. The Plant Cell 12, 2395–2408.
| Crossref |
PubMed |
Lin JH,
Li H,
Zhang Y,
Ron D, Walter P
(2009) Divergent effects of PERK and IRE1 signaling on cell viability. PLoS ONE 4, e4170.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Liu Y,
Feng X,
Xu Y,
Yu J,
Ao G,
Peng Z, Zhao Q
(2009) Overexpression of millet ZIP-like gene (SiPf40) affects lateral bud outgrowth in tobacco and millet. Plant Physiology and Biochemistry 47, 1051–1060.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Logemann J,
Schell J, Willmitzer L
(1987) Improved method for the isolation of RNA from plant tissues. Analytical Biochemistry 163, 16–20.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 Molecular Biology 54, 583–596.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
MacDiarmid CW,
Gaither LA, Eide D
(2000) Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. The EMBO Journal 19, 2845–2855.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Maser P,
Thomine S,
Schroeder JI,
Ward JM, Hirschi K ,
et al
.
(2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiology 126, 1646–1667.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Moreau S,
Thomson RM,
Kaiser BN,
Trevaskis B,
Guerinot ML,
Udvardi MK,
Puppo A, Day DA
(2002) GmZIP1 encodes a symbiosis-specific transporter in soybean. The Journal of Biological Chemistry 277, 4738–4746.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nishida S,
Mizuno T, Obata H
(2008) Involvement of histidine-rich domain of ZIP family transporter TjZNT1 in metal ion specificity. Plant Physiology and Biochemistry 46, 601–606.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pence NS,
Larsen PB,
Ebbs SD,
Letham DLD,
Lasat MM,
Garvin DF,
Eide D, Kochian LV
(2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proceedings of the National Academy of Sciences of the United States of America 97, 4956–4960.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pfaffl MW
(2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Research 29, e45.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Plaza S,
Tearall KL,
Zhao FJ,
Buchner P,
McGrath SP, Hawkesford MJ
(2007) Expression and functional analysis of metal transporter genes in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. Journal of Experimental Botany 58, 1717–1728.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ramesh SA,
Shin R,
Eide DJ, Schachtman DP
(2003) Differential metal selectivity and gene expression of two zinc transporters from rice. Plant Physiology 133, 126–134.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schikora A,
Thimm O,
Linke B,
Buckhout TJ,
Muller M, Schmidt W
(2006) Expression, localization, and regulation of the iron transporter LeIRT1 in tomato roots. Plant and Soil 284, 101–108.
| Crossref | GoogleScholarGoogle Scholar |
Taylor KM,
Morgan HE,
Johnson A, Nicholson RI
(2004) Structure-function analysis of HKE4, a member of the new LIV-1 subfamily of zinc transporters. The Biochemical Journal 377, 131–139.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vert G,
Briat JF, Curie C
(2001)
Aribidopsis IRT2 gene encodes a root-periphery iron transporter. The Plant Journal 26, 181–189.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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. The Plant Cell 14, 1223–1233.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Weber M,
Harada E,
Vess C,
Roepenack-Lahaye EV, Clemens S
(2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthese, a ZIP transporter and other genes as potential. The Plant Journal 37, 269–281.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Xia YF,
Zhao Q,
Yu JJ, Ao GM
(2005) Study of subcellular localization of PF40. Progress in Biochemistry and Biophysics 32, 1020–1025.
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.). Molecular Biology Reports 36, 281–287.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhao H, Eide D
(1996) The yeast ZRT1 gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation. Proceedings of the National Academy of Sciences of the United States of America 93, 2454–2458.
| Crossref | GoogleScholarGoogle Scholar | PubMed |