Abstract
Aims
Nickel (Ni) and zinc (Zn) interactions during their uptake and root-to-shoot translocation and the potential role of histidine therein were studied in different populations of the Ni/Zn hyperaccumulator Noccaea caerulescens and the Ni hyperaccumulator Odontarrhena corsica.
Methods
The effect of exogenous L-histidine supply on Ni and Zn uptake and translocation in N. caerulescens and O. corsica, and xylem loading in shoot-excised root systems of different N. caerulescens populations, were studied under separate and combined exposure.
Results
In O. corsica, Zn inhibited both the translocation and the uptake of Ni, whereas Ni did not significantly affect Zn uptake or translocation. In N. caerulescens, both in intact plants and shoot-excised root systems, Zn usually inhibited the uptake, but not the translocation of Ni, whereas Ni did not affect the uptake, but inhibited the translocation of Zn, though not in two populations with low Zn xylem loading capacity. Exogenous histidine supply did not significantly affect Zn translocation in O. corsica and intact plants of an ultramafic population of N. caerulescens, but enhanced Zn xylem loading in two calamine populations of N. caerulescens and Ni translocation in all of them.
Conclusions
High free L-histidine concentrations in roots might promote Ni hyperaccumulation in obligate Ni hyperaccumulators, such as O. corsica, in nature. The high histidine concentration in roots of N. caerulescens, which is primarily a Zn hyperaccumulator, might not only explain its species-wide conserved capacity to hypertranslocate Ni, but may also contribute to its Zn translocation capacity, at least in non-ultramafic populations.
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References
Alves S, Nabais C, Simões Gonçalves ML, Correia dos Santos M (2011) Nickel speciation in the xylem sap of the hyperaccumulator Alyssum serpyllifolium ssp. lusitanicum growing on serpentine soils of northeast Portugal. J Plant Physiol 168:1715–1722
Assunção AG, Martins PD, De Folter S, Vooijs R, Schat H, Aarts MGM (2001) Elevated expression of metal transporter genes in three populations of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 24:217–226
Assunção AG, Bookum WM, Nelissen HJ, Vooijs R, Schat H, Ernst WH (2003a) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419
Assunção AG, Schat H, Aarts MGM (2003b) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159:351–360
Assunção AG, Ten Bookum WM, Nelissen HJ, Vooijs R, Schat H, Ernst WH (2003c) A cosegregation analysis of zinc (Zn) accumulation and Zn tolerance in the Zn hyperaccumulator Thlaspi caerulescens. New Phytol 159:383–390
Assunção AGL, Pieper B, Vromans J, Lindhout P, Aarts MGM, Schat H (2006) Construction of a genetic linkage map of Thlaspi caerulescens and quantitative trait loci analyses of zinc accumulation. New Phytol 170:21–32
Assunção AGL, Bleeker P, Ten Bookum WM, Vooijs R, Schat H (2008) Intraspecific variation of metal preference patterns for hyperaccumulation in Thlaspi caerulescens: evidence from binary exposures. Plant Soil 303:289–299
Baker AJ, Brooks R (1989) Terrestrial higher plants which hyperaccumulate metallic elements. A review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126
Baklanov IA, Seregin IV, Ivanov VB (2009) Histochemical analysis of nickel distribution in the hyperaccumulator and excluder in the genus Alyssum L. Doklady Biol Sci 429:548–550
Becher M, Talke IN, Krall L, Krämer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268
Blindauer CA, Schmid R (2010) Cytosolic metal handling in plants: determinants for zinc specificity in metal transporters and metallothioneins. Metallomics 2:510–529
Brooks RR, Lee J, Reeves RD, Jaffré T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57
Callahan DL, Baker AJ, Kolev SD, Wedd AG (2006) Metal ion ligands in hyperaccumulating plants. J Biol Inorg Chem 11:2–12
Callahan DL, Kolev SD, O’Hair RA, Salt DE, Baker AJ (2007) Relationships of nicotianamine and other amino acids with nickel, zinc and iron in Thlaspi hyperaccumulators. New Phytol 176:836–848
Cataldo DA, Wildung RE (1978) Soil and plant factors influencing the accumulation of heavy metals by plants. Environ Health Perspect 27:149–159
Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486
Clemens S (2019) Metal ligands in micronutrient acquisition and homeostasis. Plant Cell Environ 42:2902–2912
Clemens S, Palmgren M, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315
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
Corso M, García de la Torre VS (2020) Biomolecular approaches to understanding metal tolerance and hyperaccumulation in plants. Metallomics 12:840–859
Craciun AR, Meyer CL, Chen J, Roosens N, De Groodt R, Hilson P, Verbruggen N (2012) Variation in HMA4 gene copy number and expression among Noccaea caerulescens populations presenting different levels of Cd tolerance and accumulation. J Exp Bot 63:4179–4189
Dalir N, Tandy S, Gramlich A, Khoshgoftarmanesh A, Schulin R (2017) Effects of nickel on zinc uptake and translocation in two wheat cultivars differing in zinc efficiency. Environ Exp Bot 134:96–101
Deng THB, Cloquet C, Tang YT, Sterckeman T, Echevarria G, Estrade N, Morel J-L, Qiu RL (2014) Nickel and zinc isotope fractionation in hyperaccumulating and nonaccumulating plants. Environ Sci Technol 48:11926–11933
Deng THB, Tang YT, Sterckeman T, Echevarria G, Morel JL, Qiu RL (2019) Effects of the interactions between nickel and other trace metals on their accumulation in the hyperaccumulator Noccaea caerulescens. Environ Exp Bot 158:73–79
Deniau AX, Pieper B, Ten Bookum WM, Lindhout P, Aarts MGM, Schat H (2006) QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens. Theor Appl Genet 113:907–920
Flis P, Ouerdane L, Grillet L, Curie C, Mari S, Lobinski R (2016) Inventory of metal complexes circulating in plant fluids: a reliable method based on HPLC coupled with dual elemental and high-resolution molecular mass spectrometric detection. New Phytol 211:1129–1141
Frérot H, Faucon MP, Willems G, Godé C, Courseaux A, Darracq A, Verbruggen N, Saumitou-Laprade P (2010) Genetic architecture of zinc hyperaccumulation in Arabidopsis halleri: the essential role of QTL× environment interactions. New Phytol 187:355–367
García de la Torre VS, Majorel-Loulergue C, Rigaill GJ, Alfonso-González D, Soubigou-Taconnat L, Pillon Y, Barreau L, Thomine S, Fogliani B, Burtet-Sarramegna V, Merlot S (2021) Wide cross-species RNA-Seq comparison reveals convergent molecular mechanisms involved in nickel hyperaccumulation across dicotyledons. New Phytol 229:994–1006
Gonneau C, Genevois N, Frérot H, Sirguey C, Sterckeman T (2014) Variation of trace metal accumulation, major nutrient uptake and growth parameters and their correlations in 22 populations of Noccaea caerulescens. Plant Soil 384:271–287
Halimaa P, Lin Y-F, Ahonen VH, Blane D, Clemens S, Gyenesei A, Häikiö E, Kärenlampi SO, Laiho A, Aarts MGM, Pursiheimo G-M, Schat H, Schmidt H, Tuomainen MH, Tervahauta AI (2014) Gene expression differences between Noccaea caerulescens ecotypes help indentifying candidate genes for metal phytoremediation. Environ Sci Technol 48:3344–3353
Halimaa P, Blande D, Baltzi E, Aarts MGM, Granlund L, Keinänen M, Kärenlampi SO, Kozhevnikova AD, Peräniemi S, Schat H, Seregin IV, Tuomainen M, Tervahauta AL (2019) Transcriptional effects of cadmium on iron homeostasis differ in calamine populations of Noccaea caerulescens. Plant J 97:306–320
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 453:391–396
Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506
Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, Young J, Camakaris J, Harper JF, Cobbett CS (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339
Ingle RA, Mugford ST, Rees JD, Campbell MM, Smith JAC (2005) Constitutively high expression of the histidine biosynthetic pathway contributes to nickel tolerance in hyperaccumulator plants. Plant Cell 17:2089–2106
Iqbal M, Nawaz I, Hassan Z, Hakvoort HW, Bliek M, Aarts MG, Schat H (2013) Expression of HMA4 cDNAs of the zinc hyperaccumulator Noccaea caerulescens from endogenous NcHMA4 promoters does not complement the zinc-deficiency phenotype of the Arabidopsis thaliana hma2hma4 double mutant. Front Plant Sci 4:404
Kerkeb L, Krämer U (2003) The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiol 131:716–724
Khalid BY, Tinsley J (1980) Some effects of nickel toxicity on rye grass. Plant Soil 55:139–144
Kozhevnikova AD, Seregin IV, Erlikh NT, Shevyreva TA, Andreev IM, Verweij R, Schat H (2014) Histidine-mediated xylem loading of zinc is a species-wide character in Noccaea caerulescens. New Phytol 203:508–519
Kozhevnikova AD, Seregin IV, Aarts MG, Schat H (2020) Intra-specific variation in zinc, cadmium and nickel hypertolerance and hyperaccumulation capacities in Noccaea caerulescens. Plant Soil 452:479–498
Kozhevnikova AD, Seregin IV, Zhukovskaya NV, Kartashov AV, Schat H (2021) Histidine-mediated nickel and zinc translocation in intact plants of the hyperaccumulator Noccaea caerulescens. Russ J Plant Physiol 68:S37–S50
Krämer U (2010) Metal hyperaccumulation in plants. Ann Rev Plant Biol 61:517–534
Krämer U, Cotter-Howells JD, Charnock JM, Baker AJ, Smith JA (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638
Krämer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272
Kukier U, Peters CA, Chaney RL, Angle JS, Roseberg RJ (2004) The effect of pH on metal accumulation in two Alyssum species. J Environ Qual 33:2090–2102
Küpper H, Kochian LV (2010) Transcriptional regulation of metal transport genes and mineral nutrition during acclimatization to cadmium and zinc in the Cd/Zn hyperaccumulator, Thlaspi caerulescens (Ganges population). New Phytol 185:114–129
Lasat MM, Baker AJ, Kochian LV (1998) Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens. Plant Physiol 118:875–883
Lasat MM, Pence NS, Garvin DF, Ebbs SD, Kochian LV (2000) Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. J Exp Bot 51:71–79
Lin YF, Aarts MGM (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206
Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytol 145:11–20
Merlot S (2020) Understanding nickel responses in plants: More than just an interaction with iron homeostasis. Plant Cell Physiol 61:443–444
Merlot S, García de la Torre VS, Hanikenne M (2018) Physiology and molecular biology of trace element hyperaccumulation. In: van der Ent A (ed) Agromining: Farming for Metals. Springer, Cham, pp 93–116
Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13
Milner MJ, Craft E, Yamaji N, Koyama E, Ma JF, Kochian LV (2012) Characterization of the high affinity Zn transporter from Noccaea caerulescens, NcZNT1, and dissection of its promoter for its role in Zn uptake and hyperaccumulation. New Phytol 195:113–123
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 inflate. Plant Soil 428:153–162
Mohseni R, Ghaderian SM, Schat H (2019) Nickel uptake mechanisms in two Iranian nickel hyperaccumulators, Odontarrhena bracteata and Odontarrhena inflata. Plant Soil 434:263–269
Monsant AC, Kappen P, Wang Y, Pigram PJ, Baker AJM, Tang C (2011) In vivo speciation of zinc in Noccaea caerulescens in response to nitrogen form and zinc exposure. Plant Soil 348:167–183
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
Nishida S, Aisu A, Mizuno T (2012) Induction of IRT1 by the nickel-induced iron-deficient response in Arabidopsis. Plant Signal Behav 7:329–331
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
Ouerdane L, Mari S, Czernic P, Lebrun M, Łobiński R (2006) Speciation of non-covalent nickel species in plant tissue extracts by electrospray Q-TOFMS/MS after their isolation by 2D size exclusion-hydrophilic interaction LC (SEC-HILIC) monitored by ICP-MS. J Anal Atom Spectrom 21:676–683
Palmer CM, Guerinot ML (2009) Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat Chem Biol 5:333–340
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
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. Proc Natl Acad Sci 97:4956–4960
Persans MW, Yan X, Patnoe J-MML, Krämer U, Salt DE (1999) Molecular dissection of the role of histidine in nickel hyperaccumulation in Thlaspi goesingense (Halacsy). Plant Physiol 121:1117–1126
Piccini DF, Malavolta E (1992) Effect of nickel on two common bean cultivars. J Plant Nutr 15:2343–2350
Pollard AJ, Powell KD, Harper FA, Smith JAC (2002) The genetic basis of metal hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566
Rahman H, Sabreen S, Alam S, Kawai S (2005) Effects of nickel on growth and composition of metal micronutrients in barley plants grown in nutrient solution. J Plant Nutr 28:393–404
Richau KH, Kozhevnikova AD, Seregin IV, Vooijs R, Koevoets PL, Smith JA, Ivanov VB, Schat H (2009) Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens. New Phytol 183:106–116
Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci 97:12356–12360
Salt DE, Prince RC, Baker AJM, Raskin I, Pickering IJ (1999) Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environ Sci Technol 33:713–717
Schaaf G, Honsbein A, Meda AR, Kirchner S, Wipf D, von Wirén N (2006) AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J Biol Chem 281:25532–25540
Schat H, Llugany M, Bernhard R (2000) Metal-specific pattern of tolerance, uptake, and transport of heavy metals in hyperaccumulating and non-hyperaccumulating metallophytes. In: Phytoremediation of contaminated soils and water. CRC Press LLC, pp 171–188
Seregin IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53:257–277
Seregin IV, Kozhevnikova AD (2008) Roles of root and shoot tissues in transport and accumulation of cadmium, lead, nickel, and strontium. Russ J Plant Physiol 55:1–22
Seregin IV, Kozhevnikova AD (2020) Low-molecular-weight ligands in plants: role in metal homeostasis and hyperaccumulation. Photosynth Res. https://doi.org/10.1007/s11120-020-00768-1
Seregin IV, Erlikh NT, Kozhevnikova AD (2014) Nickel and zinc accumulation capacities and tolerance to these metals in the excluder Thlaspi arvense and the hyperaccumulator Noccaea caerulescens. Russ J Plant Physiol 61:204–214
Seregin IV, Kozhevnikova AD, Zhukovskaya NV, Schat H (2015) Cadmium tolerance and accumulation in excluder Thlaspi arvense and various populations of hyperaccumulator Noccaea caerulescens. Russ J Plant Physiol 62:837–846
Seregin IV, Kozhevnikova AD, Schat H (2019) Comparison of L-histidine effects on nickel translocation into the shoots of different species of the genus Alyssum. Russ J Plant Physiol 66:340–344
Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman WH & Co, San Francisco
Sposito G (1986) Distribution of potentially hazardous trace metals. In: Singel H, Singel A (eds) Metal ions in biological systems, concept on metal ion toxicity. Marcel Dekker, New York, pp 1–20
Sterckeman T, Cazes Y, Gonneau C, Sirguey C (2017) Phenotyping 60 populations of Noccaea caerulescens provides a broader knowledge of variation in traits of interest for phytoextraction. Plant Soil 418:523–540
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
Taylor SI, Macnair MR (2006) Within and between population variation for zinc and nickel accumulation in two species of Thlaspi (Brassicaceae). New Phytol 169:505–514
van de Mortel JE, Villanueva LA, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, van Themaat EV, Koornneef M, Aarts MGM (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147
Van der Pas L, Ingle RA (2019) Towards an understanding of the molecular basis of nickel hyperaccumulation in plants. Plants 8:11
Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776
Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richaud P (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312
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
Visioli G, Gullì M, Marmiroli N (2014) Noccaea caerulescens populations adapted to grow in metalliferous and non-metalliferous soils: Ni tolerance, accumulation and expression analysis of genes involved in metal homeostasis. Environ Exp Bot 105:10–17
Williams LE, Mills RF (2005) P1B-ATPases – an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502
Wong CK, Cobbett CS (2009) HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181:71–78
Yang X, Li T, Yang J, He Z, Lu L, Meng F (2006) Zinc compartmentation in root, transport into xylem, and absorption into leaf cells in the hyperaccumulating species of Sedum alfredii Hance. Planta 224:185–195
Zemanová V, Pavlík M, Pavlíková D, Tlustoš P (2014) The significance of methionine, histidine and tryptophan in plant responses and adaptation to cadmium stress. Plant Soil Environ 60:426–432
Acknowledgements
The authors wish to thank Rudo Verweij, Rob Broekman, Richard van Logtestijn, and Riet Vooijs for technical assistance and Dr. Rufus Chaney for kindly providing the seeds of Odontarrhena corsica. This work was supported by the Russian Science Foundation Grant No. 21-14-00028 (https://rscf.ru/project/21-14-00028/). The quantification of Ni and Zn in O. corsica was partially supported by the Ministry of Science and Higher Education of the Russian Federation (state assignment № 121040800153-1).
Funding
This work was supported by the Russian Science Foundation Grant No. 21-14-00028 (https://rscf.ru/project/21-14-00028/). The quantification of Ni and Zn in O. corsica was partially supported by the Ministry of Science and Higher Education of the Russian Federation (state Assignment No. 121040800153-1).
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Kozhevnikova, A.D., Seregin, I.V. & Schat, H. Translocation of Ni and Zn in Odontarrhena corsica and Noccaea caerulescens: the effects of exogenous histidine and Ni/Zn interactions. Plant Soil 468, 295–318 (2021). https://doi.org/10.1007/s11104-021-05080-y
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DOI: https://doi.org/10.1007/s11104-021-05080-y