Startseite Effects of ZnCl2 on ROS generation, plasma membrane properties, and changes in protein expression in grapevine root explants
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Effects of ZnCl2 on ROS generation, plasma membrane properties, and changes in protein expression in grapevine root explants

  • Vladimír Repka EMAIL logo , Roderik Fiala , Milada Čiamporová und Ján Pavlovkin
Veröffentlicht/Copyright: 16. Juni 2016
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Biologia
Aus der Zeitschrift Biologia Band 71 Heft 5

Abstract

This study is aimed at the responses of grapevine adventitious root explants to zinc (Zn2+) excess. Within 24 h Zn2+ induced oxidative burst in concentration-dependent manner. The time course analysis revealed biphasic response in superoxide (O2–·) production. Hydrogen peroxide (H2O2) accumulation rose gradually within 24 h. Enhanced Zn2+ concentrations did not induce progression of cell death. Immediately upon Zn2+ addition to the perfusion solution, root epidermal cells exhibited hyperpolarization of their electrical membrane potential (EM), that was transient and independent of Zn2+ concentration. The subsequent, transient depolarization of EM was concentration-dependent and its magnitude increased with increasing Zn2+ concentration. After 24 h the EM in treated roots recovered and its values were identical with those of control roots. Membrane permeability of root cells increased in the roots treated with 5 mM Zn2+ within 24 h while the lower concentrations did not show any impact on membrane permeability. Differences in protein expression pattern identified by proteomic approach involving antibody microarray expression profiling revealed Zn2+-induced upregulation of apoptosis-related protein dolichyl-diphosphooligosaccharide-protein glycosyltransferase subunit (DAD1), extracellular signal-regulated kinase 1/2 (ERK1/2), some antioxidant enzymes and structural proteins in the roots. Moreover, the proteins involved in plant defense mechanisms endochitinase I (CHIT 1) and phenylalanine ammonia-lyase (PAL) were down-regulated indicating a cross-talk between defense and heavy metal signaling pathways. Taken together, these results showed that the grape cultivar Limberger is highly Zn2+-responsive and could be used as a model plant for studying physiological and molecular responses to heavy metal excess.

Key words: Vitis vinifera; grapevine; zinc; membrane potential (EM); protein expression; oxidative stress; cellular viability

Acknowledgements

This work was supported by grant no. 2/0023/13 from the Grant Agency VEGA, Bratislava, Slovakia.

References

Baker M.A. & Orlandi E.W. 1995. Active oxygen in plant pathogenesis. Ann. Rev. Phytopathol. 33:299-321.10.1146/annurev.py.33.090195.001503Suche in Google Scholar

Baxter A., Mittler R. & Suzuki N. 2014. ROS as key players in plant stress signalling. J. Exp. Bot. 65: 1229-1240.10.1093/jxb/ert375Suche in Google Scholar

Bazihizina B., Taiti C., Marti L., Rodrigo-Moreno A.R., Spinelli F., Giordano C., Caparrotta S., Gori M., Azzarello E. & Man-cuso S. 2014. Zn2+-induced changes at the root level account for the increased tolerance of acclimated tobacco plants. J. Exp. Bot.65: 4931-4942.10.1093/jxb/eru251Suche in Google Scholar

Békésiová B., Hraška Š., Libantová J., Moravčíková J. & Matušíková I. 2008. Heavy metal stress induced accumulation of chitinase isoforms in plants. Mol. Biol. Rep. 35: 579–588.10.1007/s11033-007-9127-xSuche in Google Scholar

Broadley M.R., White P.J., Hammond J.P., Zelko I. & Lux, A. 2007. Zinc in plants. New Phytol. 173:677-702.10.1111/j.1469-8137.2007.01996.xSuche in Google Scholar

Brotman Y., Landau U., Pnini S., Lisec J., Balazadeh S., Mueller-Roeber B., Zilberstein A., Willmitzer L., Chet I. & Viterbo A. 2012. The LysM Receptor-Like Kinase LysM RLK1 is required to activate defense and abiotic-stress responses induced by overexpression of fungal chitinases in Arabidopsis plants. Mol. Plant. 5: 1113-1124.10.1093/mp/sss021Suche in Google Scholar

Cakmak I. 2000. Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol. 146:185-205.10.1046/j.1469-8137.2000.00630.xSuche in Google Scholar

Cakmak I. & Marschner H. 1988a. Increase in membrane permeability and exudation in roots of zinc deficient plants. J. Plant Physiol. 132:356-361.10.1016/S0176-1617(88)80120-2Suche in Google Scholar

Cakmak I. & Marschner H. 1988b. Zinc-dependent changes in ESR signals, NADPH oxidase and plasma membrane permeability in cotton roots. Physiol. Plant. 73:182-186.10.1111/j.1399-3054.1988.tb09214.xSuche in Google Scholar

Chang C.T., Lo H.F., Wu C.J. & Sung H.Y. 1992. Purification and properties of chitinase from cabbage. Bioc. Int. 28:707– 715.Suche in Google Scholar

Chang H.B., Lin C.W. & Huang, H.J. 2005. Zinc-induced cell death in rice (Oryza sativa L.) roots. Plant Growth Regul. 46: 261-266.10.1007/s10725-005-0162-0Suche in Google Scholar

Chaoui A., Mazhoudi S., Ghorbal M.H. & Elferjani E. 1997. Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Sci. 127:139-147.10.1016/S0168-9452(97)00115-5Suche in Google Scholar

Colcombet J. & Hirt H. 2008. Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Bioc. J. 413:217-226.10.1042/BJ20080625Suche in Google Scholar PubMed

Deepak S., Shailasree S., Kini R., Muck A., Mithofer A. & Shetty S.H. 2010. Hydroxyproline-rich glycoproteins and plant defence. J. Phytopathol. 158:585-593.10.1111/j.1439-0434.2010.01669.xSuche in Google Scholar

de las Mercedes D.M., Pintor-Toro J.A. & Cubero B. 2006. Trans-genic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol. 142:722-730.10.1104/pp.106.086140Suche in Google Scholar PubMed PubMed Central

Ebel J. & Mithofer A. 1998. Early events in the elicitation of plant defence. Planta 206:335-348.10.1007/s004250050409Suche in Google Scholar

Farinati S., DalCorso G., Bona E., Corbella M., Lampis S., Cec-coni D., Polati R., Berta G., Vallini G. & Furini A. 2009. Proteomic analysis of Arabidopsis halleri shoots in response to the heavy metals cadmium and zinc and rhizosphere microorganisms. Proteomics 9: 4837–4850.10.1002/pmic.200900036Suche in Google Scholar PubMed

Fiala R., Repka V., Čiamporová M., Martinka M. & Pavlovkin, J. 2015. Early cadmium-induced effects on reactive oxygen species production, cell viability and membrane electrical potential in grapevine roots. Vitis 54: 175–182.Suche in Google Scholar

Hall J.I. 2002. Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 53: 1–11.10.1093/jexbot/53.366.1Suche in Google Scholar

Helmersson A., von Arnold S. & Bozhkov P.V. 2008. The level of free intracellular zinc mediates programmed cell death/cell survival decisions in plant embryos. Plant Physiol. 147:1158– 1167.10.1104/pp.108.122598Suche in Google Scholar PubMed PubMed Central

Hossain M.A., Hasanuzzaman M. & Fujita M. 2010. Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol. Molec. Biol. Plants 16: 259– 272.10.1007/s12298-010-0028-4Suche in Google Scholar PubMed PubMed Central

Ivanov Y.V., Savochkin Y.V. & Kuznetsov V.V. 2012. Scots pine as a model plant for studying the mechanisms of conifers adaptation to heavy metal action: 2. Functioning of antioxidant enzymes in pine seedlings under chronic zinc action. Russ. J. Plant Physiol. 59: 50-58.10.1134/S1021443712010098Suche in Google Scholar

Jonak C., Nakagami H. & Hirt H. 2004. Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol. 136:1–8.Suche in Google Scholar

Kasprzewska A. 2003. Plant chitinases – regulation and function. Cell. Mol. Biol. Lett. 8: 809-824.Suche in Google Scholar

Kelleher D.J. & Gilmore R. 1997. DAD1, the defender against apoptotic cell death, is a subunit of the mammalian oligosac-charyltransferase. Proc. Natl. Acad. Sci. USA 94:4994-4999.10.1073/pnas.94.10.4994Suche in Google Scholar PubMed PubMed Central

Kenderešová L., Staňová A., Pavlovkin J., Ďurišová E., Nadu-binská M., Čiamporová, M. & Ovečka, M. 2012. Early Zn2+ –induced effects on membrane potential account for primary heavy metal susceptibility in tolerant and sensitive Arabidopsis species. Ann. Bot. 110:445–459.10.1093/aob/mcs111Suche in Google Scholar PubMed PubMed Central

Kennedy C. & Gonsalves F. 1987. The action of divalent zinc, cadmium, mercury, copper and lead on the trans-root potential and H+ efflux of excised roots. J. Exp. Bot. 38:800-817.10.1093/jxb/38.5.800Suche in Google Scholar

Kobza J. 2010. Monitoring pôd Slovenska. In: Kobza J. (ed.), Soil Science and Conservation Research Institute, Bratislava, Slovakia, 38 pp.Suche in Google Scholar

Krämer U., Talke I.N. & Hanikenne M. 2007. Transition metal transport. FEBS Lett. 581:2263-2272.10.1016/j.febslet.2007.04.010Suche in Google Scholar PubMed

Le Gall H., Philippe F., Domon J.M., Gillet F., Pelloux J. & Rayon C. 2015. Cell wall metabolism in response to abiotic stress. Plants 4: 112-166.10.3390/plants4010112Suche in Google Scholar PubMed PubMed Central

Lee K.P., Kim C., Landgraf F. & Apel K. 2007. EXECUTER1-and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc. Nat. Acad. Sci. USA 104:10270-10275.10.1073/pnas.0702061104Suche in Google Scholar PubMed PubMed Central

Li X., Yang Y., Jia L., Chen H. & Wei X. 2013. Zinc-induced oxidative damage, antioxidant enzyme response and proline metabolism in roots and leaves of wheat plants. Ecotoxicol. Environ. Safety 89:150-157.10.1016/j.ecoenv.2012.11.025Suche in Google Scholar PubMed

Lin C.W., Chang H.B. & Huang H.J. 2005. Zinc induces mitogen-activated protein kinase activation mediated by reactive oxygen species in rice roots. Plant Physiol. Bioc. 43:963–968.10.1016/j.plaphy.2005.10.001Suche in Google Scholar PubMed

Liu X.M., Kim K.E., Kim K.C., Nguyen X.C., Han H.J., Jung M.S., Kim H.S., Kim S.H., Park H.C., Yun D.J. & Chung W.S. 2010. Cadmium activates Arabidopsis MPK3 and MPK6 via accumulation of reactive oxygen species. Phy-tochemistry 71:614-618.10.1016/j.phytochem.2010.01.005Suche in Google Scholar PubMed

Llamas A., Ullrich C.I. & Sanz A. 2008. Ni2+ toxicity in rice: effect on membrane functionality and plant water content. Plant Physiol. Bioch. 46: 905-910.10.1016/j.plaphy.2008.05.006Suche in Google Scholar PubMed

López-Millán A.F., Ellis D.R. & Grusak M.A. 2005. Effect of zinc and manganese supply on the activities of superoxide dismutase and carbonic anhydrase in Medicago truncatula wild type and raz mutant plants. Plant Sci. 168:1015-1022.10.1016/j.plantsci.2004.11.018Suche in Google Scholar

Lucini L. & Bernardo L. 2015. Comparison of proteome response to saline and zinc stress in lettuce. Front. Plant Sci. 6: 1–12.10.3389/fpls.2015.00240Suche in Google Scholar PubMed PubMed Central

Mirlean N., Roisenberg A. & Chies J.O. 2007. Metal contamination of vineyard soils in wet subtropics (southern Brazil). Environ. Poll. 149:10-17.10.1016/j.envpol.2006.12.024Suche in Google Scholar PubMed

Mittler R., Herr E.H., Orvar B.L., van Camp V., Willekens H., Inze D. & Ellis E.B. 1999. Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc. Nat. Acad. Sci. USA 96: 14165-14170.10.1073/pnas.96.24.14165Suche in Google Scholar PubMed PubMed Central

Morina F., Jovanovic L., Mojovic M., Vidovic M., Pankovic, Veljovic S. & Jovanovic S. 2010. Zinc-induced oxidative stress in Verbascum thapsus is caused by an accumulation of reactive oxygen species and quinhydrone in the cell wall. Physiol. Plant. 140:209-224.10.1111/j.1399-3054.2010.01399.xSuche in Google Scholar PubMed

Murashige T. & Skoog F. 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15: 473-49710.1111/j.1399-3054.1962.tb08052.xSuche in Google Scholar

Nishimura M.T. & Dangl J.L. 2010. Arabidopsis and the plant immune system. Plant J. 61: 1053-1066.10.1111/j.1365-313X.2010.04131.xSuche in Google Scholar PubMed PubMed Central

Ohki K. 1984. Zinc nutrition related to critical deficiency and toxicity levels for sorghum. Agron. J. 76: 253–256.10.2134/agronj1984.00021962007600020019xSuche in Google Scholar

Pavlovkin J., Luxová M., Mistríková I. & Mistrík I. 2006. Short-and long-term effects of cadmium on transmembrane electric potential (EM) in maize roots. Biologia 61: 109–114.10.2478/s11756-006-0016-xSuche in Google Scholar

Pavlovkin J., Fiala R., Čiamporová M., Martinka M. & Repka V. 2016. Impact of nickel on grapevine (Vitis vinifera L.) root plasma membrane, ROS generation, and cell viability. Acta Bot. Croatica 75: 25-30.10.1515/botcro-2016-0017Suche in Google Scholar

Ramos M. & López-Acevedo M. 2004. Zinc levels in vineyard soils from the Alt Penedes-Anoia region (NE Spain) after compost application. Adv. Environ. Res. 8: 687–696.10.1016/S1093-0191(03)00041-8Suche in Google Scholar

Rentel M.C., Lecourieux D., Ouaked F., Usher S. L., Petersen L., Okamoto H., Knight H., Peck S.C., Grierson C.S. & Hirt H. 2004. OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427:858–861.10.1038/nature02353Suche in Google Scholar PubMed

Repka V. 2006. Early defence responses induced by two distinct elicitors derived from a Botrytis cinerea in grapevine leaves and cell suspensions. Biol. Plantarum 50: 94–106.10.1007/s10535-005-0080-zSuche in Google Scholar

Repka V. & Čarná M. 2011. Post-transcriptional gene silencing conferred by the ectopic expression of the grapevine miRNA-g1 and inhibition of the response by anti-miRNA-g1 inhibitor. Agriculture 57: 137-143.10.2478/v10207-011-0014-zSuche in Google Scholar

Repka V., Fiala R., Čarná M. & Pavlovkin J. 2013. Membrane potential differences and viability of grapevine root cells treated with HgCl2. Plant Soil. Environ. 59: 353-358.10.17221/1/2013-PSESuche in Google Scholar

Repka V., Fiala R., Čiamporová M., Martinka M. & Pavlovkin J. 2015. Antibody microarray expression profiling of maize roots treated with cadmium and nickel. Agriculture 61: 41–49.10.1515/agri-2015-0009Suche in Google Scholar

Rojas C.M., SenthilKumar M., Wang K., Ryu C., Kaundal A. & Mysore K.S. 2012. Glycolate oxidase modulates reactive oxygen species–mediated signal transduction during non-host resistance in Nicotiana benthamiana and Arabidopsis. Plant Cell 24:336-352.10.1105/tpc.111.093245Suche in Google Scholar PubMed PubMed Central

Sagardoy R., Morales F., Lopez-Millan A., Abadia A. & Abadia . 2009. Effects of zinc toxicity on sugar beet (Beta vulgaris L.) plants grown in hydroponics. Plant Biol. 11:339–350.10.1111/j.1438-8677.2008.00153.xSuche in Google Scholar PubMed

Sheline C.T., Behrens M.M. & Choi D.W. 2000. Zinc-induced cortical neuronal death: contribution of energy failure attributable to loss of NAD+ and inhibition of glycolysis. J. Neurosci. 20:3139-3146.10.1523/JNEUROSCI.20-09-03139.2000Suche in Google Scholar

Stoyanova Z. & Doncheva S. 2002. The effect of zinc supply and succinate treatment on plant growth and mineral uptake in pea plant. Braz. J. Plant Physiol. 14:111-116.10.1590/S1677-04202002000200005Suche in Google Scholar

Tripathi B.N. & Gaur J 2004. Relationship between copper-and zinc-induced oxidative stress and proline accumulation in Scenedesmus sp. Planta 219:397–404.10.1007/s00425-004-1237-2Suche in Google Scholar PubMed

Weckx J.E.J. & Clijsters H.M.M. 1997. Zn phytotoxicity induces oxidative stress in primary leaves of Phaseolus vulgaris. Plant Physiol. Bioc. 35: 405-410.Suche in Google Scholar

White M.C., Chaney R.L. & Decker A.M. 1979. Differential cul-tivar tolerance in soybean to phytotoxic levels of soil Zn. 2. Range of Zn additions and the uptake and translocation of Zn, Mn, Fe, and P. Agron. J. 71:126-131.Suche in Google Scholar

Yakimova E.T., Kapchina-Toteva, Laarhoven L.J., Harren F.M. & Woltering E.J. 2006. Involvement of ethylene and lipid signalling in cadmium-induced programmed cell death in tomato suspension cells. Plant Physiol. Bioc. 44:581–589.10.1016/j.plaphy.2006.09.003Suche in Google Scholar PubMed

Yang Y., Su C., Yao Y., Zhang Y. & Achal V. 2011. Growth and physiological responses of grape (Vitis vinifera "Combier") to excess zinc. Acta Physiol. Plant. 33: 1483-1491.10.1007/s11738-010-0687-3Suche in Google Scholar

Yuan Q.H., Shi G.C., Zhao J., Zhang H. & Xu Q.S. 2009. Physiological and proteomic analyses of Alternanthera philoxeroides under zinc stress. Russian J. Plant Physiol. 56: 495–502.10.1134/S1021443709040086Suche in Google Scholar

Zalamena J., Melo G.W., Henrique P. Santos H.P., da Silva L.S., Fialho F.B. & Brunetto G. 2015. Physiological characterization of grapevine rootstocks grown in soil with increasing zinc doses. Rev. Bras. Eng. Agríc. Ambient. 19:973-980.10.1590/1807-1929/agriambi.v19n10p973-980Suche in Google Scholar

Abbreviations
CAT

catalase

CHIT 1

endochitinase

DAD1

dolichyl-diphosphooligosaccharide-protein glycosyltransferase subunit

EM

membrane electrical potential

ERK1/2

extracellular signal-regulated kinase 1/2

FC

fusicoccin

GOX

glycolate oxidase

H2O2

hydrogen peroxide

HM

heavy metals

HPRG

hydroxyproline-rich glycoprotein

IAA

indole-3-acetic acid

O2–·

superoxide anion radical

PAL

phenylalanine ammonia-lyase

PCD

programmed cell death

PI

propidium iodide

PM

plasma membrane

ROS

reactive oxygen species.

Received: 2016-2-15
Accepted: 2016-3-30
Published Online: 2016-6-16
Published in Print: 2016-5-1

© 2016 Institute of Botany, Slovak Academy of Sciences

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https://doi.org/10.1515/biolog-2016-0063
Schlagwörter für diesen Artikel
Vitis vinifera; grapevine; zinc; membrane potential (EM); protein expression; oxidative stress; cellular viability

Artikel in diesem Heft

  1. Cellular and Molecular Biology
  2. A broad host range food-grade cloning vector for lactic acid bacteria
  3. Cellular and Molecular Biology
  4. Antimicrobial and morphogenic effects of emodin produced by A spergillus awamori WAIR120
  5. Cellular and Molecular Biology
  6. Herbal augmentation enhances malachite green bio degradation efficacy of Saccharomyces cerevisiae
  7. Cellular and Molecular Biology
  8. Efflux pump inhibitory activity of flavonoids isolated from Alpinia calcarata against methicillin-resistant Staphylococcus aureus
  9. Cellular and Molecular Biology
  10. Status of metal pollution in rivers flowing through urban settlements at Pune and its effect on resident microflora
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  12. Use of N, N′-diacetylchitobiose in decreasing toxic effects of indoor air pollution by preventing oxidative DNA damage
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  14. The relationship between macrophyte assemblages and environmental variables in drainage and irrigation canals in Slovakia
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  16. Effects of ZnCl2 on ROS generation, plasma membrane properties, and changes in protein expression in grapevine root explants
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  18. Molecular characterization and alternative splicing of a MYB transcription factor gene in tumourous stem mustard and its response to abiotic stresses
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  20. First report of Gussevia asota (Monogenea: Dactylogyridae), destructive parasite of A stronotus ocellatus (Perciformes: Cichlidae) in Europe
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  23. Zoology
  24. Biodiversity of zooplankton (Rotifera and crustacea) in water soldier (Stratiotes aloides) habitats
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