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Nickel uptake mechanisms in two Iranian nickel hyperaccumulators, Odontarrhena bracteata and Odontarrhena inflata

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Abstract

Background and aims

Mechanisms and transporters responsible for Ni uptake in plants are largely unknown. To characterize Ni uptake mechanisms in Ni hyperaccumulators, we compared the effects of channel blockers, high Ca, high Fe, Zn, Mn, Cu, or Co, and low temperature on Ni uptake in two Iranian serpentine endemics, Odontarrhena bracteata and (two populations of) O. inflata.

Methods

Ni uptake was measured in the presence and absence of the K and Ca channel blockers, tetraethylammonium (TEA) and verapamil, respectively, at high and low Ca, and with and without (additional) Fe, Zn, Cu, Mn or Co (100 μM) in the nutrient solution. To estimate the potential contribution of passive uptake, Ni uptake was also measured at low and high temperature (4 and 25 °C).

Results

Verapamil inhibited Ni uptake by 65, 72, and 91% in O. bracteata, O. inflata from Baneh, and O. inflata from Marivan, respectively, but TEA was without effect. High Ca inhibited Ni uptake by 30 to 40%. Mn inhibited Ni uptake by about 40% in all species/populations. Fe inhibited Ni uptake, by about 30%, in O. bracteata, but not at all in O. inflata. Other metals had no effect. Low temperature decreased Ni uptake by ±70% in both species/populations.

Conclusions

In Odontarrhena Ni hyperaccumulators Ni is predominantly taken up via Ca channels. A Fe-deficiency inducible transporter contributes to Ni uptake in O. bracteata, but not in O. inflata. A relative small part of the Ni uptake in O. inflata (10–30%) remains unexplained. In any case, it is most probably neither mediated by apoplastic transport, nor by more or less specific transporters of Zn, Fe, Mn, or Co.

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References

  • Aschmann SG, Zasoski RJ (1987) Nickel and rubidium uptake by whole oat plants in solution culture. Physiol Plant 71:191–196

    Article  CAS  Google Scholar 

  • Asemaneh T, Ghaderian SM, Baker AJM (2007) Responses to Mg/Ca balance in an Iranian serpentine endemic plant, Cleome heratensis (Capparaceae) and a related non-serpentine species,C. foliolosa. Plant Soil 293:49–59

    Article  CAS  Google Scholar 

  • Assunção AGL, Martins PDAC, 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 Environ 24:217–226

    Article  Google Scholar 

  • Assunção AGL, Bookum WM, Nelissen HJ, Vooijs R, Schat H Ernst WH (2003) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419

    Article  CAS  Google Scholar 

  • Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements, a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

    CAS  Google Scholar 

  • Brown SL, Angle JS, Chaney RL, Baker AJM (1995) Zinc and cadmium uptake by hyperaccumulator Thlaspi caerulescens grown in nutrient solution. Soil Sci Soc Am J 59:125–133

    Article  CAS  Google Scholar 

  • Cataldo DA, Garland TR, Wildung RE (1978) Nickel in plants. I. Uptake kinetics using intact soybean seedlings. Plant Physiol 62:563–565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng THB, Cloquet C, Tang YT, Sterckeman T, Echevarria G, Estrade N, Morel JL, Qiu RL (2014) Nickel and zinc isotope fractionation in hyperaccumulating and non-accumulating plants. Environ Sci Technol 48:11926–11933

    Article  CAS  PubMed  Google Scholar 

  • Ghaderian SM, Mohtadi A, Rahiminejad MR, Baker AJM (2007a) Nickel and other metal uptake and accumulation by species of Alyssum (Brassicaceae) from the ultramafics of Iran. Environ Pollut 145:293–298

    Article  CAS  PubMed  Google Scholar 

  • Ghaderian SM, Mohtadi A, Rahiminejad R, Reeves RD, Baker AJM (2007b) Hyperaccumulation of nickel by two Alyssum species from the serpentine soils of Iran. Plant Soil 293:91–97

    Article  CAS  Google Scholar 

  • Ghaderian SM, Ghasemi R, Hajihashemi F (2015) Interaction of nickel and manganese in uptake, translocation and accumulation by the nickel-hyperaccumulator plant, Alyssum bracteatum (Brassicaceae). Aus J Bot 63:47–55

    Article  CAS  Google Scholar 

  • Jammes F, Hu HC, Villiers F, Bouten R, Kwak JM (2011) Calcium-permeable channels in plant cells. FEBS J 27:4262–4276

    Article  CAS  Google Scholar 

  • Liu J, Duan CQ, Zhang XH, Zhu YN Hu C (2011) Characteristics of chromium (III) uptake in hyperaccumulator Leersia hexandra Swartz. Environ Exp Bot 74:122–126

    Article  CAS  Google Scholar 

  • Lloyd J, Taylor JA (1994) On the temperature-dependence of soil respiration. Funct Ecol 8:315–323

    Article  Google Scholar 

  • Mohseni R, Ghaderian SM, Ghasemi R, Schat H (2018) Differential effects of iron starvation and iron excess on nickel uptake kinetics in two Iranian nickel hyperaccumulators, Odontarrhena bracteata and Odontarrhena inflata. Plant Soil 428:153–162

    Article  CAS  Google Scholar 

  • Nishida S, Tsuzuki C, Kato A, Aisu A, Yoshida J, Mizuno T (2011) AtIRT1, the primary iron uptake transporter in the root, mediates excess nickel accumulation in Arabidopsis thaliana. Plant Cell Physiol 52:1433–1442

    Article  CAS  PubMed  Google Scholar 

  • Nishida S, Kato A, Tsuzuki C, Yoshida J, Mizuno T (2015) Induction of nickel accumulation in response to Zinc deficiency in Arabidopsis thaliana. Int J Mol Sci 16:9420–9430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Dell RE, James JJ, Richards JH (2006) Congeneric serpentine and nonserpentine shrubs differ more in leaf ca: mg than in tolerance of low N, low P, or heavy metals. Plant Soil 280:49–64

    Article  CAS  Google Scholar 

  • Pineros M, Tester M (1995) Characterization of a voltage-dependent Ca2+-selective channel from wheat roots. Planta 195:478–488

    Article  CAS  Google Scholar 

  • Piñeros M, Tester M (1997) Calcium channels in higher plant cells: selectivity, regulation and pharmacology. J Exp Bot 48:551–577

    Article  PubMed  Google Scholar 

  • Puschenreiter M, Schnepf A, Molina MI, Fitz WJ, Horak O, Klepp J, Schrefl T, Lombi E, Wenzel WW (2005) Changes of Ni biogeochemistry in the rhizosphere of the hyperaccumulator Thlaspi goesingense. experimental evidence and modeling. Plant Soil 271:205–218

    Article  CAS  Google Scholar 

  • Redjala T, Sterckeman H, Skiker S, Echevarria G (2010) Contribution of apoplast and symplast to short term nickel uptake by maize and Leptoplax emarginata roots. Environ Exp Bot 68:99–106

    Article  CAS  Google Scholar 

  • Reeves RD, Baker AJM, Jaffré T, Erskine PD, Echevarria G, van der Ent A (2017) A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol 218:407-411

  • Shen ZG, Zhao FJ, McGrath SP (1997) Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non-hyperaccumulator Thlaspi ochroleucum. Plant Cell Environ 20:898–906

    Article  CAS  Google Scholar 

  • Sunkar R, Kaplan B, Bouche N, Arazi T, Dolev D, Talke IN, Maathuis FJ, Sanders D, Bouchez D, Fromm H (2000) Expression of a truncated tobacco NtCBP4 channel in transgenic plants and disruption of the homologous Arabidopsis CNGC1 gene confer Pb2+ tolerance. Plant J 24:533–542

    Article  CAS  PubMed  Google Scholar 

  • Tu S, Ma LQ (2005) Comparison of arsenic and phosphate uptake and distribution in arsenic hyperaccumulating and nonhyperaccumulating fern. J Plant Nutr 27:1227–1242

    Article  CAS  Google Scholar 

  • Verlière G, Heller R (1981) Effets du nickel sur la croissance des racines isolées de Leucaena leucocephala (Lam.) de Wit et caractères de son absorption. Physiol Végétale 19:263–275

    Google Scholar 

  • White PJ (1998) Calcium channels in the plasma membrane of root cells. Ann Bot 81:173–183

    Article  CAS  Google Scholar 

  • White PJ, Pineros M, Tester M, Ridout MS (2000) Cation permeability and selectivity of a root plasma membrane calcium channel. J Membr Biol 174:71–83

    Article  CAS  PubMed  Google Scholar 

  • White PJ, Whiting SN, Baker AJM, Broadley MR (2002) Does zinc move apoplastically to the xylem in roots of Thlaspi caerulescens? New Phytol 153:199–211

    Article  Google Scholar 

  • Zhang Q, Smith FA, Sekimoto H, Reid RJ (2001) Effect of membrane surface charge on nickel uptake by purified mung bean root protoplasts. Planta 213:788–793

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank the Graduate School of University of Isfahan for providing research facilities.

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Correspondence to Seyed Majid Ghaderian.

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Responsible Editor: Antony Van der Ent.

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Mohseni, R., Ghaderian, S.M. & Schat, H. Nickel uptake mechanisms in two Iranian nickel hyperaccumulators, Odontarrhena bracteata and Odontarrhena inflata. Plant Soil 434, 263–269 (2019). https://doi.org/10.1007/s11104-018-3814-3

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