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Genome-wide analysis of iron-regulated transporter 1 (IRT1) genes in plants

Abstract

Iron (Fe) is an essential micronutrient required in a number of biological processes in plant species. Fe transporters are a type of broad-range metal transporter and have different families functioning in different compartments. This study focused on iron-regulated transporter 1 (IRT1), which are mainly responsible for Fe uptake from root, in 17 selected plant species with an emphasis on Brachypodium distachyon, Chlamydomonas reinhardtii, Solanum lycopersicum and Populus trichocarpa species. All IRT1 proteins were observed to belong to the ZIP (PF02535) protein family with eight transmembrane (TM) domains, and have a similar molecular weight (33.86–42.72 kDa, except for C. reinhardtii with 65.83 kDa) and amino acid length (324-408 aa, except for C. reinhardtii with 639 aa), with pI values of 5.31–7.16. The sub-cellular localization of these proteins was predicted to be the plasma membrane. Similar exon numbers were also detected with most genes having 2–3, except for C. reinhardtii (5), Physcomitrella patens (5) and Vitis vinifera (4). In a phylogenetic tree, monocot-dicot separation was not observed in main groups but some subgroups included only monocot or dicot proteins. Predicted interaction partner analysis of AtIRT1 (AT2G30080.1) pointed to main interaction partners either directly related with iron transport or that of other metal ion. The results of this study provide a theoretical reference for elucidating the structural and biological role of IRT1 genes/proteins in plant species.

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Literature Cited

  1. Bloß, T., S. Clemens, and D. H. Nies. 2002. Characterization of the ZAT1p zinc transporter from Arabidopsis thaliana in microbial model organisms and reconstituted proteoliposomes. Planta. 214: 783–791.

    Article  PubMed  Google Scholar 

  2. Bashir, K., H. Inoue, S. Nagasaka, M. Takahashi, H. Nakanishi, S. Mori, and N.K. Nishizawa. 2006. Cloning and Characterization of deoxymugineic acid synthase genes from graminaceous plants. J. Biol. Chem. 43:32395–32402.

    Article  Google Scholar 

  3. Briat, J.F., I. Fobis-Loisy, N. Grignon, S. Lobr´eaux, N. Pascal, G. Savino, S. Thoiron, N. Von Wirén, and O. Van Wuytswinkel. 1995. Cellular and molecular aspects of iron metabolism in plants. Biol. Cell 84:69–81.

    CAS  Article  Google Scholar 

  4. Briat J.F., and S. Lobr´eaux. 1997. Iron transport and storage in plants. Trends Plant Sci. 2:187–193.

    Article  Google Scholar 

  5. Cellier, M., G. Prive, A. Belouchi, T. Kwan, V. Rodrigues, W. Chia, and P. Gros. 1995. Nramp defines a family of membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 92:10089–10093.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  6. Colangelo, E.P., and M.L. Guerinot. 2006. Put the metal to the petal: metal uptake and transport throughout plants. Curr. Opin. Plant. Biol. 9:322–330.

    CAS  Article  PubMed  Google Scholar 

  7. Curie, C., J.M. Alonso, M. Le Jean, J.R. Ecker, and J.F. Briat. 2000. Root Iron Transport Mutant 1233. Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem. J. 347:749–755.

    CAS  PubMed  Google Scholar 

  8. Eng, B.H., M.L. Guerinot, D. Eide, and Saier Jr, M.H. 1998. Sequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. J. Membrane Biol. 166:1–7.

    CAS  Article  Google Scholar 

  9. Franceschini, A., D. Szklarczyk, S. Frankild, M. Kuhn, M. Simonovic, A. Roth, J. Lin, P. Minguez, P. Bork, C.v. Mering, and L.J. Jensen. 2013. STRING v9. 1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41:808–815.

    Article  Google Scholar 

  10. Gasteiger, E., C. Hoogland, A. Gattiker, S. Duvaud, M.R. Wilkins, R.D. Appel, and A. Bairoch. 2005. Protein identification and analysis tools on the ExPASy server, p. 571–607. In: John M. Walker (ed.) The Proteomics Protocols Handbook, Humana. USA.

  11. Goodstein, D.M., S. Shu, R. Howson, R. Neupane, R.D. Hayes, J. Fazo, and D.S. Rokhsar. 2012. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40:1178–1186.

    Article  Google Scholar 

  12. Gruenheid, S., F. Canonne-Hergaux, S. Gauthier, D.J. Hackam, S. Grinstein, and P. Gros. 1999. The iron transport protein NRAMP2 is an integral membrane glycoprotein that colocalizes with transferrin in recycling endosomes. J. Exp. Med. 189:831–841.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  13. Guerinot, M.L. 2000. The ZIP family of metal transporters. Biochim. Biophys. Acta 1465:190–198.

    CAS  Article  PubMed  Google Scholar 

  14. Guo, A.Y., Q.H. Zhu, X. Chen, and J.C. Luo. 2007. GSDS: a gene structure display server. Yi Chuan 29:1023–1026.

    CAS  Article  PubMed  Google Scholar 

  15. Higuchi, K., K. Suzuki, H. Nakanishi, H. Yamaguchi, N.K. Nishizawa, and S. Mori. 1999. Cloning Of Nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol. 119:471–479.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  16. Hruz, T., Laule, O., Szabo, G., Wessendorp, F., Bleuler, S., Oertle, L., and Zimmermann, P. 2008. Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinf. 2008.

    Google Scholar 

  17. Inoue, H., T. Kobayashi, T. Nozoye, M. Takahashi, Y. Kakei, K. Suzuki, M. Nakazono, H. Nakanishi, M. Mori, and N.K. Nishizawa. 2009. Rice OsYSL15 is an iron-Regulated iron (III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J. Biol. Chem. 284: 3470–3479.

    CAS  Article  PubMed  Google Scholar 

  18. Kim, S.A. and M. L. Guerinot. 2007. Mining iron: iron uptake and transport in plants. FEBS Lett. 581:2273–2280.

    CAS  Article  PubMed  Google Scholar 

  19. Kobayashi, T. and N.K. Nishizawa. 2012. Iron uptake, translocation, and regulation in higher plants. Annu. Rev. Plant Biol. 63:131–152.

    CAS  Article  PubMed  Google Scholar 

  20. Koen, E., A. Besson-Bard, C. Duc, J. Astier, A. Gravot, P. Richaud, and D. Wendehenne. 2013. Arabidopsis thaliana nicotianamine synthase 4 is required for proper response to iron deficiency and to cadmium exposure. Plant Sci. 209:1–11.

    CAS  Article  PubMed  Google Scholar 

  21. Korshunova, Y.O., D. Eide, W.G. Clark, M.L. Guerinot, and H.B. Pakrasi. 1999. The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol. Biol. 40:37–44.

    CAS  Article  PubMed  Google Scholar 

  22. Koralewski, T.E. and K.V. Krutovsky. 2011. Evolution of exon-intron structure and alternative splicing. PLoS One, 6:e18055.

    Article  Google Scholar 

  23. Krogh, A., B. Larsson, G. von Heijne, and E.L.L. Sonnhammer. 2001. Predicting transmembraneprotein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 305: 567–580.

    CAS  Article  PubMed  Google Scholar 

  24. Kunz, H.H., M. Gierth, A. Herdean, M. Satoh-Cruz, D.M. Kramer, C. Spetea, and J.I. Schroeder. 2014. Plastidial transporters KEA1,-2, and-3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. Proc. Natl. Acad. Sci. USA. 111: 7480–7485.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  25. Lee, S., J.C. Chiecko, S.A. Kim, E.L. Walker, Y. Lee, M.L. Guerinot, and G. An. 2009a. Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol. 150:786–800.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  26. Lee, S., U.S. Jeon, S.J. Lee, Y.K. Kim, D.P. Persson, S. Husted, and G. An. 2009b. Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proc. Natl. Acad. Sci. USA. 106:22014–22019.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  27. Ma, J.F., S. Taketa, Y.C. Chang, T. Iwashita, H. Matsumoto, K. Takeda, and K. Nomoto. 1999. Genes controlling hydroxylations of phytosiderophores are located on different chromosomes in barley (Hordeum vulgare L.). Planta 207:590–596.

    CAS  Article  Google Scholar 

  28. Marschner, H. 1995. Mineral Nutrition of Higher Plants. 2nd ed., Academic press, London.

    Google Scholar 

  29. Mäser, P., S. Thomine, J.I. Schroeder, J.M. Ward, K. Hirschi, H. Sze, and M.L. Guerinot. 2001. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126: 1646–1667.

    PubMed Central  Article  PubMed  Google Scholar 

  30. Miyadate, H., S. Adachi, A. Hiraizumi, K. Tezuka, N. Nakazawa, T. Kawamoto, and H. Akagi. 2011. OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol. 189:190–199.

    CAS  Article  PubMed  Google Scholar 

  31. Nakanishi, H., I. Ogawa, Y. Ishimaru, S. Mori, and N.K. Nishizawa. 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.

    CAS  Article  Google Scholar 

  32. Nevo, Y. and N. Nelson. 2006. The NRAMP family of metaliontransporters. Biochim. Biophys. Acta 1763:609–620.

    CAS  Article  PubMed  Google Scholar 

  33. Nozoye, T., S. Nagasaka, T. Kobayashi, M. Takahashi, Y. Sato, M. Sato and N.K. Nishizawa. 2011. Phytosiderophore efflux Transporters are crucial for iron acquisition in graminaceous plants. J. Biol. Chem. 286:5446–5454.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  34. Orgad, S.A.R.A., H.A.N.N.A.H. Nelson, D.A.N.I.E.L. Segal, and N.A.T.H.A.N. Nelson. 1998. Metal ions suppress the abnormal taste behavior of the Drosophila mutant malvolio. J. Exp. Biol. 201:115–120.

    CAS  PubMed  Google Scholar 

  35. Pedas, P., C.K. Ytting, A.T. Fuglsang, T.P. Jahn, J.K. Schjoerring, and S. Husted. 2008. Manganese efficiency In barley: identification and characterization of the metal ion transporter HvIRT1. Plant Physiol. 148:455–466.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  36. Rogozin, I. B., Sverdlov, A. V., Babenko, V. N., and Koonin, E. V. 2005. Analysis of evolution of exon-intron structure of eukaryotic genes. Briefings Bioinf. 6:118–134.

    CAS  Article  Google Scholar 

  37. Romiti, M. 2010. Entrez Nucleotide and Entrez Protein FAQs. Gene 1:270.

    Google Scholar 

  38. Römheld, V. and H. Marschner. 1986. Evidence for a specific uptake system for iron phytosiderophore in roots of grasses. Plant Physiol. 80:175–180.

    PubMed Central  Article  PubMed  Google Scholar 

  39. Schaaf, G., U. Ludewig, B.E. Erenoglu, S. Mori, T. Kitahara, and N. Von Wiren. 2004. ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J. Biol. Chem. 279:9091–9096.

    CAS  Article  PubMed  Google Scholar 

  40. Smoot, M.E., Ono, K., Ruscheinski, J., Wang, P. L., and Ideker, T. 2011. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics. 27:431–432.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  41. Sonnhammer, E.L., S.R. Eddy, and R. Durbin. 1997. Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins: Struct., Funct., Genet. 28:405–420.

    CAS  Article  Google Scholar 

  42. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol. Biol. Evol. 28:2731–2739.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  43. Takahashi, M., H. Yamaguchi, H. Nakanishi, T. Shioiri, N.K. Nishizawa, and S. Mori. 1999. Cloning two Genes for nicotianamine aminotransferase, a critical enzyme in iron acquisition (Strategy II) in graminaceous plants. Plant Physiol. 121:947–956.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  44. Thomine, S. and Vert, G. 2013. Iron transport in plants: better be safe than sorry. Curr. Opin. Plant Biol. 16:322–327.

    CAS  Article  PubMed  Google Scholar 

  45. Thomine, S., R. Wang, J.M. Ward, N.M. Crawford, and J.I. Schroeder. 2000. Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc. Natl. Acad. Sci. USA. 97:4991–4996.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  46. Thompson, J.D., D.G. Higgins, and T.J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673–4680.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  47. Timothy, L., B. Mikael Bodén, F.A. Buske, M. Frith, C.E. Grant, L. Clementi, J. Ren, W.W. Li, and W.S. Noble. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37:202–208.

    Article  Google Scholar 

  48. Ueno, D., A.D. Rombol`a, T. Iwashita, K. Nomoto, and J.F. Ma. 2007. Identification of two new Phytosiderophores secreted by perennial grasses. New Phytol. 174:304–310.

    CAS  Article  PubMed  Google Scholar 

  49. Vert, G., N. Grotz, F. Dédaldéchamp, F. Gaymard, M.L. Guerinot, J.F. Briat, and C. Curie. 2002. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell Online. 14:1223–1233.

    CAS  Article  Google Scholar 

  50. Wang, M., Q. Xu, and M. Yuan. 2011. Zinc homeostasis is involved in unfolded protein response under salt stress. Plant Signal. Behav. 6:77–79.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  51. Xia, J., N. Yamaji, T. Kasai, and J.F. Ma. 2010. Plasma membranelocalized trans-Porter for aluminum in rice. Proc. Natl. Acad. Sci. U.S.A. 107:18381–18385.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  52. Yen, M.R., Y.H. Tseng, and M.H. ffixJr. Saier 2001. Maize Yellow Stripe1, an iron-phytosiderophore uptake transporter, is a member of the oligopeptide transporter (OPT) family. Microbiol. 147: 2881–2883.

    CAS  Article  Google Scholar 

  53. Yu C.S., Y.C. Chen, C.H. Lu, and J.K. Hwang. 2006. Prediction of protein subcellular localization. Proteins: struct., Funct., Bioinf. 64:643–651.

    CAS  Article  Google Scholar 

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Correspondence to Ibrahim Ilker Ozyigit.

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Vatansever, R., Filiz, E. & Ozyigit, I.I. Genome-wide analysis of iron-regulated transporter 1 (IRT1) genes in plants. Hortic. Environ. Biotechnol. 56, 516–523 (2015). https://doi.org/10.1007/s13580-015-0014-4

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Additional key words

  • chelate
  • micronutrient
  • redox reaction
  • reactive oxygen species
  • transmembrane topology