Abstract
It is well known that excessive zinc accumulation is harmful to plant cells. Though, it is uncertain at which levels of intracellular availability zinc begins to exert its deleterious action on cell physiology, as the current estimations of zinc in vitro acting concentrations seem to be non-physiologically high (micro- or millimolar). Total esterase activity in plant cells is sensitive to different adverse factors and is often used to access cell physiological activity. Therefore, we determined the effect of different zinc availability levels in vitro on the total esterase activity in extracts from rapeseed (Brassica napus L.) roots and leaves. We founded that esterase activity was drastically decreased by different protein-affecting factors, namely chaotropic salts, detergents, elevated temperatures and denaturing agents. The utilization of reaction media with exactly specified concentrations of free Zn2+ ions demonstrated that total esterase activity is substantially reduced already at tens of nM Zn2+, which is several orders of magnitude lower than was described earlier. Total phosphatase activity in extracts was even more sensitive, being drastically reduced at free Zn2+ concentrations of few nM. Therefore, the plant cellular processes can be adversely affected at very low free Zn2+ concentrations.
Similar content being viewed by others
REFERENCES
Ricachenevsky, F.K., Menguer, P.K., Sperotto, R.A., and Fett, J.P., Got to hide your Zn away: molecular control of Zn accumulation and biotechnological applications, Plant Sci., 2015, vol. 236, pp. 1–17.
Blindauer, C.A. and Schmid, R., Cytosolic metal handling in plants: determinants for zinc specificity in metal transporters and metallothioneins, Metallomics, 2010, vol. 2, pp. 510–529.
Krężel, A. and Maret, W., The biological inorganic chemistry of zinc ions, Arch. Biochem. Biophys., 2016, vol. 611, pp. 3–19.
Hara, M., Shinoda, Y., Tanaka, Y., and Kuboi, T., DNA binding of citrus dehydrin promoted by zinc ion, Plant Cell Environ., 2009, vol. 32, pp. 532–541.
Krężel, A. and Maret, W., Thionein/metallothionein control Zn(II) availability and the activity of enzymes, J. Biol. Inorg. Chem., 2008, vol. 13, pp. 401–409.
Lanquar, V., Grossmann, G., Vinkenborg, J.L., Merkx, M., Thomine, S., and Frommer, W.B., Dynamic imaging of cytosolic zinc in Arabidopsis roots combining FRET sensors and RootChip technology, New Phytol., 2014, vol. 202, pp. 198–208.
Zimmermann, M., Clarke, O., Gulbis, J.M., Keizer, D.W., Jarvis, R.S., Cobbett, C.S., Hinds, M.G., Xiao, Z., and Wedd, A.G., Metal binding affinities of Arabidopsis zinc and copper transporters: selectivities match the relative, but not the absolute, affinities of their amino-terminal domains, B-iochemistry, 2009, vol. 48, pp. 11640–11654.
Adam, S. and Murthy, S.D.S., Characterization of alterations in photosynthetic electron transport activities in maize thylakoid membranes under zinc stress, Eur. J. Exp. Biol., 2014, vol. 4, pp. 25–29.
Ghirardi, M.L., Lutton, T.W., and Seibert, M., Interactions between diphenylcarbazide, zinc, cobalt, and manganese on the oxidizing side of photosystem II, Biochemistry, 1996, vol. 35, pp. 1820–1828.
Mohanty, N., Vass, I., and Demeter, S., Impairment of photosystem 2 activity at the level of secondary quinone electron acceptor in chloroplasts treated with cobalt, nickel and zinc ions, Physiol. Plant., 1989, vol. 76, pp. 386–390.
Mathys, W., Enzymes of heavy metal-resistant and non-resistant populations of Silene cucubalus and their interaction with some heavy metals in vitro and in vivo, Physiol. Plant., 1975, vol. 33, pp. 161–165.
Bozym, R.A., Chimienti, F., Giblin, L.J., Gross, G.W., Korichneva, I., Li, Y., Libert, S., Maret, W., Parviz, M., Frederickson, C.J., and Thompson, R.B., Free zinc ions outside a narrow concentration range are toxic to a variety of cells in vitro, Exp. Biol. Med., 2010, vol. 235, pp. 741–750.
Gershater, M.C. and Edwards, R., Regulating biological activity in plants with carboxylesterases, Plant Sci., 2007, vol. 173, pp. 579–588.
Marshall, S.D., Putterill, J.J., Plummer, K.M., and Newcomb, R.D., The carboxylesterase gene family from Arabidopsis thaliana, J. Mol. Evol., 2003, vol. 57, pp. 487–500.
Víteček, J., Adam, V., Petřek, J., Vacek, J., Kizek, R., and Havel, L., Esterases as a marker for growth of BY-2 tobacco cells and early somatic embryos of the Norway spruce, Plant Cell Tissue Organ Cult., 2003, vol. 79, pp. 195–201.
Saruyama, N., Sakakura, Y., Asano, T., Nishiuchi, T., Sasamoto, H., and Kodama, H., Quantification of metabolic activity of cultured plant cells by vital staining with fluorescein diacetate, Anal. Biochem., 2013, vol. 441, pp. 58–62.
Hou, C.J., He, K., Yang, L.M., Huo, D.Q., Yang, M., Huang, S., Zhang, L., and Shen, C.H., Catalytic characteristics of plant-esterase from wheat flour, World J. Microbiol. Biotechnol., 2015, vol. 28, pp. 541–548.
Feigl, G., Lehotai, N., Molnár, Á., Ördög, A., Rodríguez-Ruiz, M., Palma, J.M., Corpas, F.J., Erdei, L., and Kolbert, Z., Zinc induces distinct changes in the metabolism of reactive oxygen and nitrogen species (ROS and RNS) in the roots of two Brassica species with different sensitivity to zinc stress, Ann. Bot., 2014, vol. 116, pp. 613–625.
Zlobin, I.E., Kartashov, A.V., and Shpakovski, G.V., Different roles of glutathione in copper and zinc chelation in Brassica napus roots, Plant Physiol. Biochem., 2017, vol. 118, pp. 333–341.
Haase, H. and Maret, W., Intracellular zinc fluctuations modulate protein tyrosine phosphatase activity in insulin/insulin-like growth factor-1 signaling, Exp. Cell Res., 2003, vol. 291, pp. 289–298.
Wilson, M., Hogstrand, C., and Maret, W., Picomolar concentrations of free zinc (II) ions regulate receptor protein-tyrosine phosphatase [beta] activity, J. Biol. Chem., 2012, vol. 287, pp. 9322–9326.
Haase, H. and Rink, L., Functional significance of zinc-related signaling pathways in immune cells, Annu. Rev. Nutr., 2009, vol. 29, pp. 133–152.
Dhindsa, R.S., Plumb-Dhindsa, P., and Thorpe, T.A., Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase, J. Exp. Bot., 1981, vol. 32, pp. 93–101.
Esen, A., A simple method for quantitative, semiquantitative, and qualitative assay of protein, Anal. Biochem., 1978, vol. 89, pp. 264–273.
Montalibet, J., Skorey, K.I., and Kennedy, B.P., Protein tyrosine phosphatase: enzymatic assays, Methods, 2005, vol. 35, pp. 2–8.
Salis, A., Bilaničová, D., Ninham, B.W., and Monduzzi, M., Hofmeister effects in enzymatic activity: weak and strong electrolyte influences on the activity of Candida rugosa lipase, J. Phys. Chem. B, 2007, vol. 111, pp. 1149–1156.
Niehaus, W.G. and Dilts, R.P., Purification and characterization of mannitol dehydrogenase from Aspergillus parasiticus, J. Bacteriol., 1982, vol. 151, pp. 243–250.
Zhao, H., Effect of ions and other compatible solutes on enzyme activity, and its implication for biocatalysis using ionic liquids, J. Mol. Catal. B: Enzym., 2005, vol. 37, pp. 16–25.
Maret, W., Inhibitory zinc sites in enzymes, Biometals, 2013, vol. 26, pp. 197–204.
Kopittke, P.M., Asher, C.J., and Menzies, N.W., Prediction of Pb speciation in concentrated and dilute nutrient solutions, Environ. Pollut., 2008, vol. 153, pp. 548–554.
Funding
The reported study was funded by Russian Foundation for Basic Research according to the research project no. 18-34-00383 mol_a.
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
The article is published in the original.
Abbreviations: FDA—fluorescein diacetate; NTA—nitrilotriacetic acid, sodium salt; TCEP—Tris(2-carboxyethyl)phosphine hydrochloride.
Rights and permissions
About this article
Cite this article
Zlobin, I.E., Kartashov, A.V. & Kuznetsov, V.V. Some Plant Enzymes Are Highly Sensitive to Inhibition by Zinc Ions. Russ J Plant Physiol 66, 591–596 (2019). https://doi.org/10.1134/S1021443719040198
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1021443719040198