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Article Addendum
Plant Signaling & Behavior 9, e29580; June; © 2014 Landes Bioscience
Histidine promotes the loading of nickel and zinc, but not of cadmium, into the xylem in Noccaea caerulescens Anna D Kozhevnikova1,*, Ilya V Seregin1, Rudo Verweij2, and Henk Schat3 1 Laboratory of Root Physiology; Timiryazev Institute of Plant Physiology; Russian Academy of Sciences; Moscow, Russia; 2Department of Animal Ecology; Faculty of Earth and Life Sciences; Vrije Universiteit Amsterdam; Amsterdam, The Netherlands; 3Department of Genetics; Faculty of Earth and Life Sciences; Vrije Universiteit Amsterdam; Amsterdam, The Netherlands
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Keywords: Noccaea caerulescens, cadmium, xylem loading, histidine, hyperaccumulation Abbreviations: CMA, Col du Mas de l’Aire; SLM, Saint Laurent le Minier *Correspondence to: Anna D Kozhevnikova; Email:
[email protected] Submitted: 05/21/2014 Revised: 06/13/2014 Accepted: 06/13/2014 Published Online: 06/18/2014 Citation: Kozhevnikova AD, Seregin IV, Verweij R, Schat H. Histidine promotes the loading of nickel and zinc, but not of cadmium, into the xylem in Noccaea caerulescens. Plant Signaling & Behavior 2014; 9:e29580; PMID: 24941070; http://dx.doi.org/10.4161/psb.29580 Addendum to: Kozhevnikova AD, Seregin IV, Erlikh NT, Shevyreva TA, Andreev IM, Verweij R, Schat H. Histidine-mediated xylem loading of zinc is a species-wide character in Noccaea caerulescens. New Phytol 2014; 203: 508–519 http://dx.doi. org/10.1111/nph.12816, PMID:24750120
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istidine is known to be involved in Ni hyperaccumulation. Recently, histidine-dependent xylem loading of Ni and Zn has been demonstrated in the Zn/ Ni/Cd hyperaccumulator, Noccaea caerulescens. Here we tested the hypothesis whether Cd xylem loading is histidinedependent, too. In contrast to that of Ni and Zn, the xylem loading of Cd was not affected by exogenous histidine. Histidine accumulation in root cells appears to facilitate the radial transport of Ni and Zn, but not Cd, across the roots. This may be due to the relatively high preference of Cd for coordination with sulfur over coordination with nitrogen, in comparison with Ni and Zn. Noccaea caerulescens F.K. Mey (previously Thlaspi caerulescens J. and C. Presl) is a Zn/Ni/Cd hyperaccumulator with considerable intra-specific genetic variation regarding the metal-specific accumulation and tolerance traits. However, all of its accessions show an extraordinary high rate of root-to-shoot translocation of all of these metals, in comparison with non-hyperaccumulators.1 The mechanisms of heavy metal hyperaccumulation are incompletely known to date. In N. caerulescens there seem to be multiple, partly accession-specific, and metalspecific accumulation and translocation mechanisms, as suggested by QTL analyses of segregating intra-specific N. caerulescens crosses,2,3 and inter-accession transcriptome comparisons.4 Just like Ni-hyperaccumulating Alyssum, N. caerulescens exhibits high
concentrations of non-protein histidine in its roots and xylem sap,5-7 and Ni-histidine coordination has been demonstrated in roots, xylem, and leaves in these and other hyperaccumulators.5,8-10 Since the majority of Ni in hyperaccumulators is coordinated with carboxylic acids, usually citrate, or malate,8-11 it is likely that histidine is involved in the plant-internal transport of Ni, rather than its final storage, usually in the vacuoles of large epidermal cells of leaves and stems.12-14 Exogenous histidine supply has been shown to promote the root-to-shoot translocation of Ni through enhancing its loading into the xylem,6,7 rather than through binding it within the xylem itself. Chelation during xylem transport seems to be required neither for Ni hyperaccumulation,15,16 nor for Zn and Cd hyperaccumulation.17,18 Richau et al.7 found that the uptake of Ni into energized tonoplast vesicles was strongly inhibited in N. caerulescens, but not in the non-hyperaccumulator reference species, Thlaspi arvense, when Ni was supplied in combination with histidine, in comparison with citrate, or sulfate salt. They suggested that histidine serves to suppress the vacuolar retention of Ni in root cell vacuoles, particularly in the inner cortex and the endodermis, in N. caerulescens. In this scenario, the high rate of Ni xylem loading in this species would be achieved through a combination of enhanced histidine accumulation in the root cell cytoplasm with a loss of the ability to transport the Ni-histidine
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Figure 1. Cadmium concentration in root pressure exudates (A) and volume of root pressure exudates (B) of N. caerulescens plants (CMA and SLM accessions) treated with half-strength Hoagland’s nutrient solution supplied with 1 µM Cd overnight after 4-h pretreatment of their roots with 1 mM L-His, L-Ala, or MES/KOH-buffered demineralized water (pH 5.5) ( = unpretreated). Values are the means of 3 replicates with 6 plants per replicate ± SE. The experimental design was as described for Ni in Richau et al.7 and Zn in Kozhevnikova et al.19 The plants were grown on Cd-free half-strength Hoagland’s nutrient solution for 8 wk prior to the experiment. The absence of significant changes in the volume of exuded xylem sap after the exogenous amino acid supply (B) indicates that there were no changes in sap production which could influence the metal concentration in it.
complex across the tonoplast. This would promote the radial transport of Ni across the root into the stele. Recently, we studied the effects of exogenous histidine on Zn xylem loading and Zn uptake into tonoplast vesicles in N. caerulescens.19 The results compared well with those obtained for Ni. Exogenous histidine enhanced the xylem loading of Zn, even more strongly than that of Ni, and inhibited Zn uptake in tonoplast vesicles, albeit only when supplied at a 2-fold higher molar concentration than Zn in N. caerulescens, while these effects were not found in T. arvense. Histidine-promoted xylem loading of Zn, in comparison with that of Ni, was less accession-specific, and less dependent on Zn exposure levels. Since Zn hyperaccumulation, in contrast to Ni hyperaccumulation, is species-wide in N. caerulescens, and because Zn hyperaccumulation is more common than Ni hyperaccumulation among Noccaea species,20 it is well possible that it evolved as a component trait of the Zn hyperaccumulation syndrome, rather than the Ni one. Here we also studied the effect of exogenous histidine on Cd xylem loading in 2 Cd-hyperaccumulating N. caerulescens accessions from lead mines in SouthFrance, SLM, and CMA. Our results
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clearly demonstrated that the Cd concentrations in the root pressure exudates and the total xylem Cd loads, in sharp contrast with those of Ni and Zn, were unaffected, occasionally even inhibited, by exogenous histidine (Figs. 1A and 2). This was shown both in plants exposed to Cd overnight and in plants grown in the presence of Cd for 8 wk prior to the experiment. The reason for this lies probably in the metals’ relative binding affinities for amino and thiol groups. While Ni and Zn have relatively high affinities for N-based chelators, Cd prefers S-based ones.21 In accordance with this, the stability of the Cd-histidine complex is much lower than those of the Zn-histidine or Ni-histidine complexes.22 In agreement with this, at least in hyperaccumulators, but probably also in most other plants, both Ni6,8-10 and Zn23 are predominantly coordinated with O and N, whereas Cd is largely coordinated with O and S, but barely or not with N.24,25 Because hyperaccumulators barely accumulate phytochelatins upon Cd exposure,26,27 it seems likely that glutathione (GSH) is their predominant low-molecular-weight, non-vacuolar Cd chelator. Since GSH has high affinity toward Cd, and is present at a high concentration in the cytoplasm, it is unlikely that exogenous histidine supply would lead to
Plant Signaling & Behavior
the formation of a Cd-histidine complex, which would in turn explain the absence of histidine-promoted Cd xylem loading. As demonstrated by Richau and Schat,28 there is a significant genetic correlation between the capacities to hyperaccumulate Zn and Ni among segregating F2 and F3 progenies of a N. caerulescens inter-accession cross. This implies that there must be common genetic determinants of Zn and Ni hyperaccumulation. It is not likely that these common determinants are involved in histidine-mediated xylem loading, since there is no considerable inter-accession variation of root histidine concentrations, neither in vacuolar Ni transport capacities.7 In addition, the ultimate step in the xylem loading process, that is, efflux of the metal from the xylem parenchyma into the vessels, is probably different for both metals. The loading of Zn is ultimately mediated by the P1B-type ATPase, HMA4, but that of Ni is most likely not.4,29 Therefore, correlated variation in Zn and Ni accumulation capacities seems to reflect common transporters for root uptake, rather than common translocation mechanisms. Likewise, root-to-shoot Zn and Cd fluxes appeared to be genetically correlated within a segregating F2 progeny of a N. caerulescens inter-accession cross.30
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Figure 2. Cd concentration (nmol ml-1) in root pressure exudates (A) and Cd xylem loading, recalculated as a percentage of total root Cd burden (B) in CMA and SLM accessions of N. caerulescens treated overnight with nutrient solution without Cd (-Cd) or nutrient solution with 1 µM Cd (+Cd), after 4-h pretreatment of their roots with 1 mM L-His, or MES/KOH-buffered demineralized water (pH 5.5) ( = unpretreated). Before the experiment the plants were grown on a half-strength Hoagland’s nutrient solution containing 1 µM Cd for 8 wk. * = significantly different from corresponding control at P < 0.05. The experimental design was as described for Zn in Kozhevnikova et al.19
However, although the xylem loading of both Zn and Cd is ultimately mediated by HMA4,29 it is likely that this genetic correlation relied on common genetic determinants for root uptake, rather than xylem loading, because the parent accessions differed strongly in their capacities for Zn and Cd uptake, but showed very similar levels of HMA4 expression.30 In conclusion, histidine accumulation in root cells seems to facilitate the radial transport of Ni and Zn across the roots in N. caerulescens. The mechanisms enabling efficient radial transport of Cd are elusive yet. Disclosure of Potential Conflicts of Interest
No potential conflicts of interest were disclosed. Acknowledgments
This work was supported by grants from the Dutch Organization for Scientific Research (NWO, 047.017.008) and the Russian Foundation for Basic Research (RFBR, No 11–04–00513).
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19. Kozhevnikova AD, Seregin IV, Erlikh NT, Shevyreva TA, Andreev IM, Verweij R, Schat H. Histidinemediated xylem loading of zinc is a species-wide character in Noccaea caerulescens. New Phytol 2014; 203: 508–19. http://dx.doi.org/10.1111/nph.12816. PMID:24750120 20. Koch MA, German DA. Taxonomy and systematics are key to biological information: Arabidopsis, Eutrema (Thellungiella), Noccaea and Schrenkiella (Brassicaceae) as examples. Front Plant Sci 2013; 4:267; PMID:23914192; http://dx.doi. org/10.3389/fpls.2013.00267 21. Singel H, Singel A. Metal ions in biological systems. Concepts on metal ion toxicity. Vol. 20. New York: Marcel Dekker, 1986, 416 p. 22. Sóvágó I, Várnagy K. Cadmium (II) Complexes of Amino Acids and Peptides. In: Cadmium: From Toxicity to Essentiality. Series: Metal Ions in Life Sciences, Vol. 11. Sigel, Astrid, Sigel, Helmut, Sigel, Roland KO, eds. 2013, 560 p. 23. Salt DE, Prince RC, Baker AJM, Raskin I, Pickering IJ. Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environ Sci Technol 1999; 33:713-7; http://dx.doi.org/10.1021/es980825x 24. Vogel-Mikuš K, Arčon I, Kodre A. Complexation of cadmium in seeds and vegetative tissues of the cadmium hyperaccumulator Thlaspi praecox as studied by X-ray absorption spectroscopy. Plant Soil 2010; 331:439-51; http://dx.doi.org/10.1007/ s11104-009-0264-y 25. Huguet S, Bert V, Laboudigue A, Barthes V, Isaure MP, Llorens I, Schat H, Sarret G. Cd speciation and localization in the hyperaccumulator Arabidopsis halleri. Environ Exp Bot 2012; 82:54-65; http:// dx.doi.org/10.1016/j.envexpbot.2012.03.011
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26. Ebbs S, Lau I, Ahner B, Kochian L. Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens (J. & C. Presl). Planta 2002; 214:635-40; PMID:11925047; http://dx.doi.org/10.1007/ s004250100650 27. Schat H, Llugany M, Vooijs R, Hartley-Whitaker J, Bleeker PM. The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. J Exp Bot 2002; 53:2381-92; PMID:12432030; http://dx.doi.org/10.1093/jxb/ erf107 28. Richau KH, Schat H. Intraspecific variation of nickel and zinc accumulation and tolerance in the hyperaccumulator Thlaspi caerulescens. Plant Soil 2009; 314:253-62; http://dx.doi.org/10.1007/ s11104-008-9724-z 29. Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Krämer U. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 2008; 453:391-5; PMID:18425111; http:// dx.doi.org/10.1038/nature06877 30. Xing JP, Jiang RF, Ueno D, Ma JF, Schat H, McGrath SP, Zhao FJ. Variation in root-to-shoot translocation of cadmium and zinc among different accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox. New Phytol 2008; 178:315-25; PMID:18266619; http://dx.doi. org/10.1111/j.1469-8137.2008.02376.x
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