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Expression of TpNRAMP5, a metal transporter from Polish wheat (Triticum polonicum L.), enhances the accumulation of Cd, Co and Mn in transgenic Arabidopsis plants

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Abstract

Main conclusion

TpRNAMP5 is mainly expressed in the plasma membrane of roots and basal stems. It functions as a metal transporter for Cd, Mn and Co accumulation.

Numerous natural resistance-associated macrophage proteins (NRAMPs) have been functionally identified in various plant species, including Arabidopsis, rice, soybean and tobacco, but no information is available on NRAMP genes in wheat. In this study, we isolated a TpNRAMP5 from dwarf Polish wheat (DPW, Triticum polonicum L.), a species with high tolerance to Cd and Zn. Expression pattern analysis revealed that TpNRAMP5 is mainly expressed in roots and basal stems of DPW. TpNRAMP5 was localized at the plasma membrane of Arabidopsis leaf protoplast. Expression of TpNRAMP5 in yeast significantly increased yeast sensitivity to Cd and Co, but not Zn, and enhanced Cd and Co concentrations. Expression of TpNRAMP5 in Arabidopsis significantly increased Cd, Co and Mn concentrations in roots, shoots and whole plants, but had no effect on Fe and Zn concentrations. These results indicate that TpNRAMP5 is a metal transporter enhancing the accumulation of Cd, Co and Mn, but not Zn and Fe. Genetic manipulation of TpNRAMP5 can be applied in the future to limit the transfer of Cd from soil to wheat grains, thereby protecting human health.

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Abbreviations

DPW:

Dwarf Polish wheat

IRT:

Iron-regulated transporter

NRAMP:

Natural resistance-associated macrophage protein

References

  • Agorio A, Giraudat J, Bianchi MW, Marion J, Espagne C, Castaings L, Lelievre F, Curie C, Thomine S, Merlot S (2017) Phosphatidylinositol 3-phosphate-binding protein AtPH1 controls the localization of the metal transporter NRAMP1 in Arabidopsis. Proc Natl Acad Sci USA 114:3354–3363

    Article  Google Scholar 

  • Barberon M, Dubeaux G, Kolb C, Isono E, Zelazny E, Vert G (2014) Polarization of IRON-REGULATIED TRANSOPRTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis. Proc Natl Acad Sci USA 111:8293–8298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barras F, Fontecave M (2011) Cobalt stress in Escherichia coli and Salmonella enterica: molecular bases for toxicity and resistance. Metallomics 3:1130–1134

    Article  CAS  PubMed  Google Scholar 

  • Cai Y, Jia T, Lam SK, Ding Y, Gao C, San MWY, Pimpl P, Jiang L (2011) Multiple cytosolic and transmembrane determinants are required for the trafficking of SCAMP1 via an ER-Golgi-TGN-PM pathway. Plant J 65:882–896

    Article  CAS  PubMed  Google Scholar 

  • Cailliatte R, Lapeyre B, Briat JF, Mari S, Curie C (2009) The NRAMP6 metal transporter contributes to cadmium toxicity. Biochem J 422:217–228

    Article  CAS  PubMed  Google Scholar 

  • Cailliatte R, Schikora A, Briat JF, Mari S, Curie C (2010) High-affinity manganese uptake by the metal transporter NRMAP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22:904–917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castaings L, Caquot A, Loubet S, Curie C (2016) The high-affinity metal transporters NRAMP1 and IRT1 team up to take up iron under sufficient metal provision. Sci Rep 6:37222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chesworth W (1991) Geochemistry of micronutrients. In: Mortvedt JJ, Cox FR, Shuman LM, Welch RM (eds) Micronutrients in agriculture, 2nd edn. Soil Science Society of America, Madison, pp 1–30

    Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Curie C, Alonso JM, Le Jean M, Ecker JR, Briat JF (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347:749–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao H, Xie W, Yang C, Xu J, Li J, Wang H, Chen X, Huang C (2018) Nramp2, a trans-Golgi network-localized manganese transporter, is required for Arabidopsis root growth under manganese deficiency. New Phytol 217:179–193

    Article  CAS  PubMed  Google Scholar 

  • Grant CA, Clarke JM, Duguid S, Chaney RL (2008) Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 390:301–310

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, Senoura T, Hase Y, Arao T, Nishizawa NK, Nakanishi H (2012) Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc Natl Acad Sci USA 109:19166–19171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K, Ono K, Yano M, Ishikawa S, Arao T, Nakanishi H, Nishizawa N (2012a) Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci Rep 2:286

    Article  PubMed  PubMed Central  Google Scholar 

  • Ishimaru Y, Bashir K, Nakanishi H, Nishizawa NK (2012b) OsNRAMP5, a major player for constitutive iron and manganese uptake in rice. Plant Signal Behav 7:763–766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaiser BN, Moreau S, Castelli J, Thomson R, Lambert A, Bogliolo S, Puppo A, Day DA (2003) The soybean NRAMP homologue, GmDMT1, is a symbiotic divalent metal transporter capable of ferrous iron transport. Plant J 35:295–304

    Article  CAS  PubMed  Google Scholar 

  • Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol Biol 40:37–44

    Article  CAS  PubMed  Google Scholar 

  • Lanquar V, Lelièvre F, Bolte S, Hamès C, Alcon C, Neumann D, Vansuyt G, Curie C, Schröder A, Krämer U, Barbier-Brygoo H, Thomine S (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24:4041–4051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lanquar V, Ramos MS, Lelièvre F, Barbier-Brygoo H, Krieger-Liszkay A, Krämer U, Thomine S (2010) Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiol 152:1986–1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Liu J, Dong D, Jia X, McCouch SR, Kochian LV (2014) Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that play a key role in rice aluminum tolerance. Proc Natl Acad Sci USA 111:6503–6508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milner MJ, Seamon J, Craft E, Kochian LV (2013) Transport properties of membranes of the ZIP family in plants and their role in Zn and Mn homeostasis. J Exp Bot 64:369–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizuno T, Usui K, Horie K, Nosaka S, Mizuno N, 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

    Article  CAS  PubMed  Google Scholar 

  • Morel M, Grouzet J, Gravot A, Auroy P, Leonhardt N, Vavasseur A, Richaud P (2009) AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol 149:894–904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morrissey J, Baxter I, Lee J, Li L, Lahner B, Grotz N, Kaplan J, Salt DE, Guerinot ML (2009) The ferroportin metal efflux proteins functions in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21:3326–3338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa NK (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

    Article  CAS  Google Scholar 

  • Nevo Y, Nelson N (2006) The NRAMP family of metal-ion transporters. BBA-Mol Cell Res 1763:609–620

    CAS  Google Scholar 

  • Nogawa K, Tsuritani I, Kido T, Honda R, Yamada Y, Ishizaki M (1987) Mechanism for bone disease found in inhabitants environmentally exposed to cadmium: decreased serum 1α, 25-dihydroxyvitamin D level. Int Arch Occ Env Hea 59:21–30

    Article  CAS  Google Scholar 

  • Oomen RJFJ, Wu J, Lelièvre F, Blanchet S, Richaud P, Barbier-Brygoo H, Aarts MGM, Thomine S (2008) Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol 181:637–650

    Article  PubMed  Google Scholar 

  • Pedas P, Ytting CK, Fuglsang AT, Jahn TP, Schjoerring JK, Husted S (2008) Manganese efficiency in barley: identification and characterization of the metal ion transporter HvIRT1. Plant Physiol 148:455–466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peris-Peris C, Serra-Cardona A, Sánchez-Sanuy F, Campo S, Ariño J, San Segundo B (2017) Two NRAMP6 isoforms function as iron and manganese transporters and contribute to disease resistance in rice. Mol Plant Microbe In 30:385–398

    Article  CAS  Google Scholar 

  • Pottier M, Oomen R, Picco C, Giraudat J, Scholz-Starke J, Richaud P, Carpaneto A, Thomine S (2015) Identification of mutations allowing natural resistance associated macrophage proteins (NRAMP) to discriminate against cadmium. Plant J 83:625–637

    Article  CAS  PubMed  Google Scholar 

  • Qin L, Han P, Chen L, Walk TC, Li Y, Hu X, Xie L, Liao H, Liao X (2017) Genome-wide identification and expression analysis of NRAMP family genes in soybean (Glycine Max L.). Front Plant Sci 8:1436

    Article  PubMed  PubMed Central  Google Scholar 

  • Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Socha AL, Guerinot ML (2014) Mn-euvering manganese: the role of transporter gene gamily membranes in manganese uptake and mobilization in plant. Front Plant Sci 5:106

    Article  PubMed  PubMed Central  Google Scholar 

  • Stinson LJ, Darmon AJ, Dagnino L, D’Souza SJ (2003) Delayed apoptosis post-cadmium injury in renal proximal tubule epithelial cells. Am J Nephrol 23:27–37

    Article  CAS  PubMed  Google Scholar 

  • Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK (2011) The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot 62:4843–4850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang Z, Cai H, Li J, Lv Y, Zhang W, Zhao F (2017) Allelic variation of NtNramp5 associated with cultivar variation in cadmium accumulation in tobacco. Plant Cell Physiol 58:1583–1593

    Article  PubMed  Google Scholar 

  • Tejada-Jiménez M, Castro-Rodríguez R, Kryvoruchko I, Lucas MM, Udvardi M, Imperial J, González-Guerrero M (2015) Medicago truncatula natural resistance-associate macrophage protein1 is required for iron uptake by rhizobia-infected nodule cells. Plant Physiol 168:258–272

    Article  PubMed  PubMed Central  Google Scholar 

  • The International Wheat Genome Sequencing Consortium (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:1251788

    Article  Google Scholar 

  • Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomine S, Lelièvre F, Debarbieus E, Schroeder JI, Barbier-Brygoo H (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34:685–695

    Article  CAS  PubMed  Google Scholar 

  • Tiwari M, Sharma D, Dwivedi S, Singh M, Tripathi RD, Trivedi PK (2014) Expression in Arabidopsis and cellular localization reveal involvement of rice NRAMP, OsNRAMP1, in arsenic transport and tolerance. Plant Cell Environ 37:140–152

    Article  CAS  PubMed  Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372

    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  PubMed Central  Google Scholar 

  • Vidal SM, Malo D, Vogan K, Skamene E, Gros P (1993) Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell 73:469–485

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Yu K, Poysa V, Shi C, Zhou Y (2012) A single point mutation in GmHMA3 affects cadmium (Cd) translocation and accumulation in soybean seeds. Mol Plant 5:1154–1156

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Wang X, Gu M, Kang H, Zeng J, Fan X, Sha L, Zhang H, Yu K, Zhou Y (2015) Cloning and characterization of four SnRK2 genes from Triticum polonicum. Biol Plant 59:211–219

    Article  CAS  Google Scholar 

  • Wang Y, Wang C, Wang X, Peng F, Wang R, Jiang Y, Zeng J, Fan X, Kang H, Sha L, Zhang H, Xiao X, Zhou Y (2016) De novo sequencing and characterization of the transcriptome of dwarf polish wheat (Triticum polonicum L.). Int. J Genomics 2016:5781412

    Google Scholar 

  • Wang X, Wang C, Sheng H, Wang Y, Zeng J, Kang H, Fan X, Sha L, Zhang H, Zhou Y (2017) Transcriptome-wide identification and expression analysis of ABC transporters in dwarf polish wheat under metal stresses. Biol Plant 61:293–304

    Article  CAS  Google Scholar 

  • Wu D, Yamaji N, Yamane M, Kashino-Fujii M, Sato K, Ma JF (2016) The HvNRAMP5 transporter mediates uptake of cadmium and manganese, but not iron. Plant Physiol 172:1899–1910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia J, Yamaji N, Kasai T, Ma J (2010) Plasma membrane-localized transporter for aluminum in rice. Proc Natl Acad Sci USA 107:18381–18385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao H, Yin L, Xu X, Li T, Han Z (2008) The iron-regulated transporter, MbNRAMP1, isolated from Malus baccata is involved in Fe, Mn and Cd trafficking. Ann Bot 102:881–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaji N, Sasaki A, Xia J, Yokosho K, Ma J (2013) A node-based switch for preferential distribution of manganese in rice. Nat Commun 4:2442

    Article  PubMed  Google Scholar 

  • Yang M, Zhang W, Dong H, Zhang Y, Lu K, Wang D, Lian X (2013) OsNRAMP3 is a vascular bundles-specific manganese transporter that is responsible for manganese distribution in rice. PLoS ONE 8:e83990

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang M, Zhang Y, Zhang L, Hu J, Zhang X, Lu K, Dong H, Wang D, Zhao F, Huang C, Lian X (2014) OsNRAMP5 contributes to manganese translocation and distribution in rice shoots. J Exp Bot 65:4849–4861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank the National Natural Science Foundation of China (No. 31470305 and 31671688) for all financial support. We thank Barbara Goodson, PhD, from Liwen Bianji, Edanz Group, China (http://www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.

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Correspondence to Yi Wang.

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Peng, F., Wang, C., Zhu, J. et al. Expression of TpNRAMP5, a metal transporter from Polish wheat (Triticum polonicum L.), enhances the accumulation of Cd, Co and Mn in transgenic Arabidopsis plants. Planta 247, 1395–1406 (2018). https://doi.org/10.1007/s00425-018-2872-3

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