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Differential effects of iron starvation and iron excess on nickel uptake kinetics in two Iranian nickel hyperaccumulators, Odontarrhena bracteata and Odontarrhena inflata

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Abstract

Aims

To characterize Ni hyperaccumulation mechanisms in naturally Ni-hyperaccumulating Odontarrhena species, Ni uptake kinetics, and the effect of Fe starvation and Fe or Zn excess thereon, were investigated in the Iranian serpentine endemics O. bracteata (one population) and O. inflata (two populations).

Methods

Plants were exposed to a series of Ni concentrations for 4 h, and Ni uptake rates were plotted against the Ni concentration in the solution. Kinetic parameters, Km and Vmax, were calculated from Lineweaver-Burke plots.

Results

Ni uptake consistently showed Michaelis–Menten kinetics. Under normal Fe supply the Km was not significantly different between species or populations, however, the Vmax was 3-fold higher in O. bracteata and O. inflata from Baneh than in O. inflata from Marivan. The rate of Ni translocation to the shoot was similar in all of the species/populations. Fe starvation (1 wk) significantly increased the Vmax for Ni uptake in O. bracteata, but not in O. inflata, and a very similar increase in Fe uptake capacity in all the species/populations. Fe excess in the nutrient solution significantly increased the Km for Ni uptake in O. bracteata, but not in O. inflata. Zn excess in the nutrient solution (300 μM) marginally inhibited Ni uptake in O. inflata, but not in O. bracteata.

Conclusions

Ni uptake seems to proceed via a Fe deficiency-inducible Fe transporter in O. bracteata, but not in O. inflata. Ni root-to-shoot translocation seems to be mediated by a Fe deficiency-inducible Fe translocation mechanism in all of the species/populations.

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References

  • Adamidis GC, Aloupi M, Kazakou E, Dimitrakopoulos PG (2014) Intra-specific variation in Ni tolerance, accumulation and translocation patterns in the Ni-hyperaccumulator Alyssum lesbiacum. Chemosphere 95:496–502

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Assunção AGL, Bleeker P, Bookum WM, Vooijs R, Schat H (2008) Intraspecific variation of metal preference patterns for hyperaccumulation in Thlaspi caerulescens: evidence from binary metal exposures. Plant Soil 303:289–299

    Article  CAS  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 

  • 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 

  • 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 

  • Baker AJM, Reeves RD, McGrath SP (1991) In situ decontamination of heavy metal polluted soils using crops of metal-accumulating plants—a feasibility study. In: situ bioreclamation, pp 600–605

    Chapter  Google Scholar 

  • Broadhurst CL, Chaney RL (2016) Growth and metal accumulation of an Alyssum murale nickel Hyperaccumulator ecotype co-cropped with Alyssum montanum and perennial ryegrass in serpentine soil. Front Plant Sci 7:451

    Article  PubMed  PubMed Central  Google Scholar 

  • Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Dioscorides Press, Portland OR

    Google Scholar 

  • Brooks RR (1998) Plants that hyperaccumulate heavy metals. CAB International, Wallingford UK

    Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Conte SS, Walker EL (2011) Transporters contributing to iron trafficking in plants. Mol Plant 4:464–476

    Article  PubMed  CAS  Google Scholar 

  • Cornu JY, Deinlein U, Höreth S, Braun M, Schmidt H, Weber M, Persson DP, Husted S, Schjoerring JK, Clemens S (2015) Contrasting effects of nicotianamine synthase knockdown on zinc and nickel tolerance and accumulation in the zinc/cadmium hyperaccumulator Arabidopsis halleri. New Phytol 206:738–750

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Elbaz B, Knaani S, David-Assael O, Mizrachy-Dagri M, Saul H, Brook E, Berezin I, Shaul O (2006) High expression in leaves of the zinc hyperaccumulator Arabidopsis halleri of AhMHX, a homolog of an Arabidopsis thaliana vacuolar metal/proton exchanger. Plant Cell Environ 29:1179–1190

    Article  PubMed  CAS  Google Scholar 

  • Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol 48:1081–1091

    Article  PubMed  CAS  Google Scholar 

  • Gendre D, Czernic P, Conéjéro G, Pianelli K, Briat JF, Lebrun M, Mari S (2007) TcYSL3, a member of the YSL gene family from the hyper-accumulator Thlaspi caerulescens, encodes a nicotianamine-Ni/Fe transporter. The. Plant J 49:1–15

    Article  PubMed  CAS  Google Scholar 

  • Gerendás J, Sattelmacher B (1997) Significance of Ni supply for growth, urease activity and the concentrations of urea, amino acids and mineral nutrients of urea-grown plants. Plant Soil 190:153–162

    Article  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  PubMed  CAS  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 

  • Ghasemi R, Ghaderian SM, Krämer U (2009) Interference of nickel with copper and iron homeostasis contributes to metal toxicity symptoms in the nickel hyperaccumulator plant Alyssum inflatum. New Phytol 184:566–580

    Article  PubMed  CAS  Google Scholar 

  • Gustin JL, Loureiro ME, Kim D, Na G, Tikhonova M, Salt DE (2009) MTP1-dependent Zn sequestration into shoot vacuoles suggests dual roles in Zn tolerance and accumulation in Zn-hyperaccumulating plants. The Plant J 57:1116–1127

    Article  PubMed  CAS  Google Scholar 

  • Halimaa P, Lin YF, Ahonen VH, Blande D, Clemens S, Gyenesei A, Häikiö E, Kärenlampi SO, Laiho A, Aarts MG Pursiheimo JP (2014) Gene expression differences between Noccaea caerulescens ecotypes help to identify candidate genes for metal phytoremediation. Environ Sci Technol 48:3344–3353

    Article  PubMed  CAS  Google Scholar 

  • Hanikenne M, Nouet C (2011) Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics. Curr Opin Plant Biol 14:252–259

    Article  PubMed  CAS  Google Scholar 

  • Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Krämer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395

    Article  PubMed  CAS  Google Scholar 

  • Huang JW, Cunningham SD (1996) Lead phytoextraction: species variation in lead uptake and translocation. New Phytol 134:75–84

    Article  CAS  Google Scholar 

  • Jammes F, Hu HC, Villiers F, Bouten R, Kwak JM (2011) Calcium-permeable channels in plant cells. The FEBS J 278:4262–4276

    Article  PubMed  CAS  Google Scholar 

  • Kim YY, Yang YY, Lee Y (2002) Pb and cd uptake in rice roots. Physiol Plant 116:368–372

    Article  CAS  Google Scholar 

  • Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Zhao H, Wu L, Liu A, Zhao FJ, Xu W (2017) Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytol 215:687–698

    Article  PubMed  CAS  Google Scholar 

  • Lombi E, Tearall KL, Howarth JR, Zhao FJ, Hawkesford MJ, McGrath SP (2002) Influence of iron status on cadmium and zinc uptake by different ecotypes of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 128:1359–1367

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lombi E, Zhao FJ, McGrath SP, Young SD, Sacchi GA (2001) Physiological evidence for a high-affinity cadmium transporter highly expressed in a Thlaspi caerulescens ecotype. New Phytol 149:53–60

    Article  CAS  Google Scholar 

  • Merlot S, Hannibal L, Martins S, Martinelli L, Amir H, Lebrun M, Thomine S (2014) The metal transporter PgIREG1 from the hyperaccumulator Psychotria gabriellae is a candidate gene for nickel tolerance and accumulation. J Exp Bot 65:1551–1564

    Article  PubMed  CAS  Google Scholar 

  • Milner MJ, Mitani-Ueno N, Yamaji N, Yokosho K, Craft E, Fei Z, Ebbs S, Clemencia Zambrano M, Ma JF, Kochian LV (2014) Root and shoot transcriptome analysis of two ecotypes of Noccaea caerulescens uncovers the role of NcNramp1 in cd hyperaccumulation. Plant J 78:398–410

    Article  PubMed  CAS  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  PubMed  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  PubMed  CAS  Google Scholar 

  • Oomen RJ, Wu J, Lelièvre F, Blanchet S, Richaud P, Barbier-Brygoo H, Aarts MG, Thomine S (2009) Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol 181:637–650

    Article  PubMed  CAS  Google Scholar 

  • Papoyan A, Kochian LV (2004) Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol 136:3814–3823

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pence NS, Larsen PB, Ebbs SD, Letham DL, Lasat MM, Garvin DF, Eide D, Kochian LV (2000) The molecular physiology of heavy metal transport in the Zn/cd hyperaccumulator Thlaspi caerulescens. Pro Nat Acad Sci 97(9):4956–4960

    Article  CAS  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 (2000) Metal-accumulating plants. In: Phytoremediation of toxic metals using plants to clean up the environment. Wiley, New York, pp 193–229

    Google Scholar 

  • Reeves RD (2006) Hyperaccumulation of trace elements by plants. In Phytoremediation of metal-contaminated soils. Springer, Dordrecht, pp 25–52

    Google Scholar 

  • Reeves RD, Brooks RR, Dudley TR (1983) Uptake of nickel by species of Alyssum, Bornmuellera, and other genera of old world Tribus Alysseae. Taxon 32:184–192

    Article  Google Scholar 

  • Richau KH, Schat H (2009) Intraspecific variation of nickel and zinc accumulation and tolerance in the hyperaccumulator Thlaspi caerulescens. Plant Soil 314:253–262

    Article  CAS  Google Scholar 

  • Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Nati Acad Sci 97:12356–12360

    Article  CAS  Google Scholar 

  • Seregin IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53:257–277

    Article  CAS  Google Scholar 

  • Talke IN, Hanikenne M, Krämer U (2006) Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 142:148–167

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van der Ent A, AJM B, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction Plant Soil. 362:319–334

  • 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. Physiologie Végétale 19:263–275

    Google Scholar 

  • Vert G, Grotz N, Dédaldéchamp 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  PubMed  PubMed Central  CAS  Google Scholar 

  • Weber M, Harada E, Vess C, Roepenack-Lahaye EV, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281

    Article  PubMed  CAS  Google Scholar 

  • Yanqun Z, Yuan L, Jianjun C, Haiyan C, Li Q, Schvartz C (2005) Hyperaccumulation of Pb, Zn and cd in herbaceous grown on lead–zinc mining area in Yunnan, China. Environ Int 31:755–762

    Article  PubMed  CAS  Google Scholar 

  • Yanqun Z, Yuan L, Schvartz C, Langlade L, Fan L (2004) Accumulation of Pb, cd, cu and Zn in plants and hyperaccumulator choice in Lanping lead–zinc mine area, China. Environ Int 30:567–576

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

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

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Authors and Affiliations

  1. Department of Biology, Faculty of Sciences, University of Isfahan, Isfahan, 81746-73441, Iran

    Roshanak Mohseni & Seyed Majid Ghaderian

  2. Department of Biology, Faculty of Sciences, Payame Noor University, Tehran, 19395-4697, Iran

    Rasoul Ghasemi

  3. Department of Ecological Science, Faculty of Earth and Life Sciences, Vrije Universiteit, De Boelelaan 1085, 1081, HV, Amsterdam, The Netherlands

    Henk Schat

Authors
  1. Roshanak Mohseni
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  2. Seyed Majid Ghaderian
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  3. Rasoul Ghasemi
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  4. Henk Schat
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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., Ghasemi, R. et al. 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 (2018). https://doi.org/10.1007/s11104-018-3666-x

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  • DOI: https://doi.org/10.1007/s11104-018-3666-x

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