Abstract
The work dealt with the influence of free L-histidine on nickel (Ni) translocation into the shoots of the hyperaccumulator plants Alyssum murale, A. fallacinum, A. corsicum, A. tenium, A. lesbiacum, A. bertolonii, A. pintodasilvae, and A. obovatum and of the closely related non-hyperaccumulator Aurinia saxatilis (formerly Alyssum saxatile). The Ni concentration in the xylem sap was determined by graphite furnace or flame atomic absorption spectrophotometry. If plants were not treated with L-histidine or L-alanine, the highest Ni concentration was found in the xylem sap of A. murale and A. corsicum. When the plants were pretreated with L‑histidine, the Ni loading into the xylem vessels increased in only two hyperaccumulator species, A. pintodasilvae and A. obovatum, and in the non-hyperaccumulator A. saxatilis. The plant pretreatment with L-alanine did not increase the Ni level in the xylem sap. This indicates that the stimulation of Ni xylem loading is histidine-specific and not characteristic of any amino acid. Therefore, the role of histidine in the selective nickel accumulation in the shoots may considerably differ even in closely related plant species of one genus. This may presumably be accounted for by both different contents of endogenous histidine in the roots and specific patterns of the metal transport and distribution in different species.

Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.REFERENCES
Brooks, R.R., Lee, J., Reeves, R.D., and Jaffré, T., Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants, J. Geochem. Explor., 1977, vol. 7, pp. 49–57.
Reeves, R.D. and Baker, A.J.M., Metal-accumulating plants, in Phytoremediation of Toxic Metals Using Plants to Clean Up the Environment, Raskin, I. and Ensley, B.D., Eds., New York: John Wiley and Sons, 2000, pp. 193–229.
Verbruggen, N., Hermans, C., and Schat, H., Molecular mechanisms of metal hyperaccumulation in plants, New Phytol., 2009, vol. 181, pp. 759–776.
Krämer, U., Metal hyperaccumulation in plants, Annu. Rev. Plant Biol., 2010, vol. 61, pp. 517–534.
Koch, M. and Al-Shehbaz, I.A., Phylogeny of Brassica and wild relatives, in Biology and Breeding of Crucifers, Gupta, S.K., Ed., Boca Raton: Taylor and Francis Group, 2009, pp. 1–19.
Cecchi, L., Gabbrielli, R., Arnetoli, M., Gonnelli, C., Hasko, A., and Selvi, F., Evolutionary lineages of nickel hyperaccumulation and systematics in European Alysseae (Brassicaceae): evidence from nrDNA sequence data, Ann. Bot., 2010, vol. 106, pp. 751–767.
Seregin, I.V. and Kozhevnikova, A.D., Physiological role of nickel and its toxic effects on higher plants, Russ. J. Plant Physiol., 2006, vol. 53, pp. 257–277.
Leitenmaier, B. and Küpper, H., Compartmentation and complexation of metals in hyperaccumulator plants, Front. Plant Sci., 2013, vol. 4, pp. 1–13.
Richau, K.H., Kozhevnikova, A.D., Seregin, I.V., Vooijs, R., Koevoets, P.L.M., Smith, J.A.C., Ivanov, V.B., and Schat, H., Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator, Thlaspi caerulescens, New Phytol., 2009, vol. 183, pp. 106–116.
Kozhevnikova, A.D., Seregin, I.V., Erlikh, N.T., Shevyreva, T.A., Andreev, I.M., Verweij, R., and Schat, H., Histidine-mediated xylem loading of zinc is a species-wide character in Noccaea caerulescens, New Phytol., 2014, vol. 203, pp. 508–519.
Kozhevnikova, A.D., Seregin, I.V., Verweij, R., and Schat, H., Histidine promotes the loading of nickel and zinc, but not of cadmium, into the xylem in Noccaea caerulescens, Plant Signal. Behav., 2014, vol. 9: e29580. http://www.tandfonline.com/doi/full/10.4161/psb.29580
Kerkeb, L. and Krämer, U., The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea, Plant Physiol., 2003, vol. 131, pp. 716–724.
Krämer, U., Cotter-Howells, J.D., Charnock, J.M., Baker, A.J.M., and Smith, A.C., Free histidine as a metal chelator in plants that accumulate nickel, Nature, 1996, vol. 379, pp. 635–638.
Assunção, A.G.L., Bookum, W.M., Nelissen, H.J.M., Vooijs, R., Schat, H., and Ernst, W.H.O., Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types, New Phytol., 2003, vol. 159, pp. 411–419.
Lasat, M.M., Baker, A.J.M., and Kochian, L.V., 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., 1998, vol. 118, pp. 875–883.
Ingle, R.A., Mugford, S.T., Rees, J.D., Campbell, M.M., and Smith, J.A.C., Constitutively high expression of the histidine biosynthetic pathway contributes to nickel tolerance in hyperaccumulator plants, Plant Cell, 2005, vol. 17, pp. 2089–2106.
Seregin, I.V. and Kozhevnikova, A.D., Roles of root and shoot tissues in transport and accumulation of cadmium, lead, nickel, and strontium, Russ. J. Plant Physiol., 2008, vol. 55, pp. 1–22.
Baklanov, I.A., Seregin, I.V., and Ivanov, V.B., Histochemical analysis of nickel distribution in the hyperaccumulator and excluder in the genus Alyssum L., Dokl. Biol. Sci., 2009, vol. 429, pp. 548–550.
Haydon, M.J. and Cobbett, C.S., Transporters of ligands for essential metal ions in plants, New Phytol., 2007, vol. 174, pp. 499–506.
Hussain, D., Haydon, M.J., Wang, Y., Wong, E., Sherson, S.M., Young, J., Camakaris, J., Harper, J.F., and Cobbett, C.S., P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis, Plant Cell, 2004, vol. 16, pp. 1327–1339.
Hanikenne, M., Talke, I.N., Haydon, M.J., Lanz, C., Nolte, A., Motte, P., Kroymann, J., Weigel, D., and Krämer, U., Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4, Nature, 2008, vol. 453, pp. 391–395.
Bernard, C., Roosens, N., Czernic, P., Lebrun, M., and Verbruggen, N., A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens, FEBS Lett., 2004, vol. 569, pp. 140–148.
Salt, D.E., Prince, R.C., Baker, A.J., Raskin, I., and Pickering, I.J., Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy, Environ. Sci. Technol., 1999, vol. 33, pp. 713–717.
Monsant, A.C., Kappen, P., Wang, Y., Pigram, P.J., Baker, A.J., and Tang, C., In vivo speciation of zinc in Noccaea caerulescens in response to nitrogen form and zinc exposure, Plant Soil, 2011, vol. 348, pp. 167–183.
Kersten, W.J., Brooks, R.R., Reeves, R.D., and Jaffre, T., Nature of nickel complexes in Psychotria douarrei and other nickel-accumulating plants, Phytochemistry, 1980, vol. 19, pp. 1963–1965.
Vacchina, V., Mari, S., Czernic, P., Marquès, L., Pianelli, K., Schaumlöffel, D., Lebrun, M., and Łobiński, R., Speciation of nickel in a hyperaccumulating plant by high-performance liquid chromatography-inductively coupled plasma mass spectroscopy and electrospray MS/MS assisted by cloning using yeast complementation, Anal. Chem., 2003, vol. 75, pp. 2740–2745.
Kim, S., Takahashi, M., Higuchi, K., Tsunoda, K., Nakanishi, H., Yoshimura, E., Mori, S., and Nishizawa, N.K., Increased nicotianamine biosynthesis confers enhanced tolerance of high levels of metals, in particular nickel, to plants, Plant Cell Physiol., 2005, vol. 46, pp. 1809–1818.
Sagner, S., Kneer, R., Wanner, G., Cosson, J.-P., Deus-Neumann, B., and Zenk, M.H., Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminata, Phytochemistry, 1998, vol. 47, pp. 339–343.
Dawson, R.M.C., Elliott, D.C., Elliott, W.H., and Jones, K.M., Data for Biochemical Research, Oxford: Clarendon, 1986.
ACKNOWLEDGMENTS
The work was partially supported by the Russian Foundation for Basic Research, project no. 15-04-02236, and by the LOCOMET International Scientific P-rogram. We are grateful to Prof. A.J.М. Baker (Melbourne, Australia) for kindly providing the seeds of the Alyssum murale, A. fallacinum, A. corsicum, A. tenium, A. lesbiacum, A. bertolonii, A. pintodasilvae, and Aurinia saxatilis; to Dr. M.N. Kataeva (Komarov Botanical Institute, Russian Academy of Sciences, St. Petersburg) for kindly providing the seeds of A. obovatum; and to Prof. V.B. Ivanov (Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Moscow) for the critical discussion of the results.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.
Additional information
Translated by A. Aver’yanov
The authors contributed equally to this work.
Rights and permissions
About this article
Cite this article
Seregin, I.V., Kozhevnikova, A.D. & Schat, H. 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 (2019). https://doi.org/10.1134/S1021443719020122
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1021443719020122


