Effect of Arsenic Soil Contamination on Stress Response Metabolites, 5-Methylcytosine Level and CDC25 Expression in Spinach

. 2023 Jun 29 ; 11 (7) : . [epub] 20230629

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37505533

Grantová podpora
CZ.02.1.01/0.0/0.0/16_019/0000845 European Union
SV21-4-21110 Ministry of Education, Youth and Sports of the Czech Republic

Experimental spinach plants grown in soil with (5, 10 and 20 ppm) arsenic (As) contamination were sampled in 21 days after As(V) contamination. Levels of As in spinach samples (from 0.31 ± 0.06 µg g-1 to 302.69 ± 11.83 µg g-1) were higher in roots and lower in leaves, which indicates a low ability of spinach to translocate As into leaves. Species of arsenic, As(III) and As(V), were represented in favor of the As (III) specie in contaminated variants, suggesting enzymatic arsenate reduction. In relation to predominant As accumulation in roots, changes in malondialdehyde levels were observed mainly in roots, where they decreased significantly with growing As contamination (from 11.97 ± 0.54 µg g-1 in control to 2.35 ± 0.43 µg g-1 in 20 ppm As). Higher values in roots than in leaves were observed in the case of 5-methylcytosine (5-mC). Despite that, a change in 5-mC by As contamination was further deepened in leaves (from 0.20 to 14.10%). In roots of spinach, expression of the CDC25 gene increased by the highest As contamination compared to the control. In the case of total phenolic content, total flavonoid content, total phenolic acids content and total antioxidant capacity were higher levels in leaves in all values, unlike the roots.

Zobrazit více v PubMed

Bradl H.B. Heavy Metals in the Environment: Origin, Interaction and Remediation. Elsevier; Amsterdam, The Netherlands: 2005.

Paul N.P., Galván A.E., Yoshinaga-Sakurai K., Rosen B.P., Yoshinaga M. Arsenic in medicine: Past, present and future. Biometals. 2023;36:283–301. doi: 10.1007/s10534-022-00371-y. PubMed DOI PMC

Upadhyay M.K., Shukla A., Yadav P., Srivastava S. A review of arsenic in crops, vegetables, animals and food products. Food Chem. 2019;276:608–618. doi: 10.1016/j.foodchem.2018.10.069. PubMed DOI

European Food Safety Authority. Arcella D., Cascio C., Gomez Ruiz J.A. Chronic dietary exposure to inorganic arsenic. EFSA J. 2021;19:50. PubMed PMC

Clemens S., Ma J.F. Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu. Rev. Plant Biol. 2016;67:489–512. doi: 10.1146/annurev-arplant-043015-112301. PubMed DOI

Nagajyoti P.C., Lee K.D., Sreekanth T.V.M. Heavy metals, occurrence and toxicity for plants: A review. Environ. Chem. Lett. 2010;8:199–216. doi: 10.1007/s10311-010-0297-8. DOI

Maciaszczyk-Dziubinska E., Wawrzycka D., Wysocki R. Arsenic and Antimony Transporters in Eukaryotes. Int. J. Mol. Sci. 2012;13:3527–3548. doi: 10.3390/ijms13033527. PubMed DOI PMC

Pandhair V., Sekhon B.S. Reactive oxygen species and antioxidants in plants: An overview. J. Plant Biochem. Biotechnol. 2006;15:71–78. doi: 10.1007/BF03321907. DOI

Zaman K.P., Pardini R.S. An Overview of the Relationship between Oxidative Stress and Mercury and Arsenic. Toxic Subst. Mech. 1996;15:151–181.

Sharma I. Arsenic induced oxidative stress in plants. Biologia. 2012;67:447–453. doi: 10.2478/s11756-012-0024-y. DOI

Souri Z., Karimi N., Sandalio L.M. Arsenic Hyperaccumulation Strategies: An Overview. Front. Cell Dev. Biol. 2017;5:67. doi: 10.3389/fcell.2017.00067. PubMed DOI PMC

Shi H., Shi X., Liu K.J. Oxidative mechanism of arsenic toxicity and carcinogenesis. Mol. Cell. Biochem. 2004;255:67–78. doi: 10.1023/B:MCBI.0000007262.26044.e8. PubMed DOI

Yalcinkaya T., Uzilday B., Ozgur R., Turkan I., Mano J. Lipid peroxidation-derived reactive carbonyl species (RCS): Their interaction with ROS and cellular redox during environmental stresses. Environ. Exp. Bot. 2019;165:139–149. doi: 10.1016/j.envexpbot.2019.06.004. DOI

Mano J., Biswas M.S., Sugimoto K. Reactive Carbonyl Species: A Missing Link in ROS Signaling. Plants. 2019;8:391. doi: 10.3390/plants8100391. PubMed DOI PMC

Nadarajah K.K. ROS Homeostasis in Abiotic Stress Tolerance in Plants. Int. J. Mol. Sci. 2020;21:5208. doi: 10.3390/ijms21155208. PubMed DOI PMC

Michalak A. Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol. J. Environ. Stud. 2006;15:523–530.

Heim K.E., Tagliaferro A.R., Bobilya D.J. Flavonoid antioxidants: Chemistry, metabolism, and structure-activity relationships. J. Nutr. Biochem. 2002;13:572–584. doi: 10.1016/S0955-2863(02)00208-5. PubMed DOI

Khanam U.K.S., Oba S., Yanase E., Murakami Y. Phenolic Acids, flavonoids and Total Antioxidant Capacity of Selected Leafy Vegetables. J. Funct. Foods. 2012;4:979–987. doi: 10.1016/j.jff.2012.07.006. DOI

Lukens L.N., Zhan S. The plant genome’s methylation status and response to stress: Implications for plant improvement. Curr. Opin. Plant Biol. 2007;10:317–322. doi: 10.1016/j.pbi.2007.04.012. PubMed DOI

Chen M., Lv S., Meng Y. Epigenetic performers in plants. Dev. Growth Differ. 2010;52:555–566. doi: 10.1111/j.1440-169X.2010.01192.x. PubMed DOI

Grativol C., Hemerly A.S., Ferreira P.C.G. Genetic and Epigenetic Regulation of Stress Responses in Natural Plant Populations. Biochim. Biophys. Acta-Gene Regul. Mech. 2012;1819:176–185. doi: 10.1016/j.bbagrm.2011.08.010. PubMed DOI

Kohli R.M., Zhang Y. TET Enzymes, TDG and the Dynamics of DNA Demethylation. Nature. 2013;502:472–479. doi: 10.1038/nature12750. PubMed DOI PMC

Shen L., Wu H., Diep D., Yamaguchi S., D’Alessio A.C., Fung H.L., Zhang K., Zhang Y. Genome-Wide Analysis Reveals TET- and TDG-Dependent 5-Methylcytosine Oxidation Dynamics. Cell. 2013;153:692–706. doi: 10.1016/j.cell.2013.04.002. PubMed DOI PMC

Meiqiong T., Jiao Y., Zhen H., Yali H., Zengqiang L., Dengjie L., Shan C., Hui Z., Jiao P., Xia W., et al. Physiological and DNA methylation analysis provides epigenetic insights into chromium tolerance in kenaf. J. Exp. Bot. 2022;194:104684.

Espinas N.A., Saze H., Saijo Y. Epigenetic control of defense signaling and priming in plants. Front. Plant Sci. 2016;7:1201. doi: 10.3389/fpls.2016.01201. PubMed DOI PMC

Thiebaut F., Hemerly A.S., Ferreira P.C.G. A Role for Epigenetic Regulation in the Adaptation and Stress Responses of Non-Model Plants. Front. Plant Sci. 2019;10:246. doi: 10.3389/fpls.2019.00246. PubMed DOI PMC

Bossdorf O., Arcuri D., Richards C.L., Pigliucci M. Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana. Evol. Ecol. 2010;24:541–553. doi: 10.1007/s10682-010-9372-7. DOI

Iwase Y., Shiraya T., Takeno K. Flowering and Dwarfism Induced by DNA Demethylation in Pharbitis Nil. Physiol. Plant. 2010;139:118–127. doi: 10.1111/j.1399-3054.2009.01345.x. PubMed DOI

Ba Q., Zhang G., Wang J., Niu N., Ma S., Wang J. Gene expression and DNA methylation alterations in chemically induced male sterility anthers in wheat (Triticum aestivum L.) Acta Physiol. Plant. 2014;36:503–512. doi: 10.1007/s11738-013-1431-6. DOI

Lechat M.M., Brun G., Montiel G., Véronési C., Simier P., Thoiron S., Pouvreau J.B., Delavault P. Seed response to strigolactone is controlled by abscisic acid-independent DNA methylation in the obligate root parasitic plant, Phelipanche ramosa L. Pomel. J. Exp. Bot. 2015;66:3129–3140. doi: 10.1093/jxb/erv119. PubMed DOI PMC

Campos N.V., Araújo T.O., Arcanjo-Silva S., Freitas-Silva L., Azevedo A.A., Nunes-Nesi A. Arsenic hyperaccumulation induces metabolic reprogramming in Pityrogramma calomelanos to reduce oxidative stress. Physiol. Plant. 2016;157:135–146. doi: 10.1111/ppl.12426. PubMed DOI

Ent A., Baker A.J.M., Reeves R.D., Pollard A.J., Schat H. Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant Soil. 2013;362:319–334.

Fayiga A.O., Saha U.K. Arsenic hyperaccumulating fern: Implications for remediation of arsenic contaminated soils. Geoderma. 2016;284:132–143. doi: 10.1016/j.geoderma.2016.09.003. DOI

Rascio N., Navari-Izzo F. Heavy Metal Hyperaccumulating Plants: How and Why Do They Do It? And What Makes Them so Interesting? Plant Sci. 2011;180:169–181. doi: 10.1016/j.plantsci.2010.08.016. PubMed DOI

Zhao F.J., McGrath S.P., Meharg A.A. Arsenic as a Food Chain Contaminant: Mechanisms of Plant Uptake and Metabolism and Mitigation Strategies. Annu. Rev. Plant Biol. 2010;61:535–559. doi: 10.1146/annurev-arplant-042809-112152. PubMed DOI

Mendoza-Cózatl D.G., Jobe T.O., Hauser F., Schroeder J.I. Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr. Opin. Plant Biol. 2011;14:554–562. doi: 10.1016/j.pbi.2011.07.004. PubMed DOI PMC

Duan G.L., Zhou Y., Tong Y.P., Mukhopadhyay R., Rosen B.P., Zhu Y.G. A CDC25 homologue from rice functions as an arsenate reductase. New Phytol. 2007;174:311–321. doi: 10.1111/j.1469-8137.2007.02009.x. PubMed DOI

Bleeker P.M., Hakvoort H.W., Bliek M., Souer E., Schat H. Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcus lanatus. Plant J. 2006;45:917–929. doi: 10.1111/j.1365-313X.2005.02651.x. PubMed DOI

Ellis D.R., Gumaelius L., Indriolo E., Pickering I.J., Banks J.A., Salt D.E. A novel arsenate reductase from the arsenic hyperaccumulating fern Pteris vittata. Plant Physiol. 2006;141:1544–1554. doi: 10.1104/pp.106.084079. PubMed DOI PMC

Dhankher O.P., Rosen B.P., McKinney E.C., Meagher R.B. Hyperaccumulation of arsenic in the shoots of Arabidopsis silenced for arsenate reductase (ACR2) Proc. Natl. Acad. Sci. USA. 2006;103:5413–5418. doi: 10.1073/pnas.0509770102. PubMed DOI PMC

Sanchez-Bermejo E., Castrillo G., del Llano B., Navarro C., Zarco-Fernandez S., Martinez-Herrera D.J., del Puerto Y.L., Munoz R., Camara C., Paz-Ares J., et al. Natural variation in arsenate tolerance identifies an arsenate reductase in Arabidopsis thaliana. Nat. Commun. 2014;5:4617. doi: 10.1038/ncomms5617. PubMed DOI

Kerk D., Templeton G., Moorhead G.B. Evolutionary radiation pattern of novel protein phosphatases revealed by analysis of protein data from the completely sequenced genomes of humans, green algae, and higher plants. Plant Physiol. 2008;146:351–367. doi: 10.1104/pp.107.111393. PubMed DOI PMC

Saleem M.H., Mfarrej M.F.B., Alatawi A., Mumtaz S., Imran M., Ashraf M.A., Rizwan M., Usman K., Ahmad P., Ali S. Silicon enhances morpho-physio-biochemical responses in arsenic stressed spinach (Spinacia oleracea L.) by minimizing its uptake. J. Plant Growth Regul. 2023;42:2053–2072. doi: 10.1007/s00344-022-10681-7. DOI

Zemanová V., Pavlíková D., Hnilička F., Pavlík M. Arsenic toxicity-induced physiological and metabolic changes in the shoots of Pteris cretica and Spinacia oleracea. Plants. 2021;10:2009. doi: 10.3390/plants10102009. PubMed DOI PMC

Cui S., Wang Z., Li X., Wang H., Wang H., Chen W. A comprehensive assessment of heavy metal(loid) contamination in leafy vegetables grown in two mining areas in Yunnan, China—A focus on bioaccumulation of cadmium in Malabar spinach. Environ. Sci. Pollut. Res. 2022;30:14959–14974. doi: 10.1007/s11356-022-23017-5. PubMed DOI

Sun Y., Mfarrej B.F., Song X., Ma J., Min B., Chen F. New insights in to the ameliorative effects of zinc and iron oxide nanoparticles to arsenic stressed spinach (Spinacia oleracea L.) Plant Physiol. Biochem. 2023;199:107715. doi: 10.1016/j.plaphy.2023.107715. PubMed DOI

Agarwal A., Gupta S.D., Barman M., Mitra A. Photosynthetic apparatus plays a central role in photosensitive physiological acclimations affecting spinach (Spinacia oleracea L.) growth in response to blue and red photon flux ratios. Environ. Exp. Bot. 2018;156:170–182. doi: 10.1016/j.envexpbot.2018.09.009. DOI

Zaheer I.E., Ali S., Saleem M.H., Ali M., Riaz M., Javed S., Sehar A., Abbas Z., Rizwan M., El-Sheikh M.A., et al. Interactive role of zinc and iron lysine on Spinacia oleracea L. growth, photosynthesis and antioxidant capacity irrigated with tannery wastewater. Physiol. Mol. Biol. Plants. 2020;26:2435–2452. doi: 10.1007/s12298-020-00912-0. PubMed DOI PMC

Zaheer I.E., Ali S., Saleem M.H., Noor I., El-Esawi M.A., Hayat K., Rizwan M., Abbas Z., El-Sheikh M.A., Alyemeni M.N. Iron–Lysine Mediated Alleviation of Chromium Toxicity in Spinach (Spinacia oleracea L.) Plants in Relation to Morpho-Physiological Traits and Iron Uptake When Irrigated with Tannery Wastewater. Sustainability. 2020;12:6690. doi: 10.3390/su12166690. DOI

Chaturvedi R., Favas P.J.C., Pratas J., Varun M., Paul M.S. Metal(loid) induced toxicity and defense mechanisms in Spinacia oleracea L. Ecological hazard and prospects for phytoremediation Ecotox. Environ. Saf. 2019;183:109570. doi: 10.1016/j.ecoenv.2019.109570. PubMed DOI

Zubair M., Khan Q.U., Mirza N., Sarwar R., Khan A.A., Baloch M.S., Fahad S., Shah A.N. Physiological response of spinach to toxic heavy metal stress. Environ. Sci. Pollut. Res. 2019;26:31667–31674. doi: 10.1007/s11356-019-06292-7. PubMed DOI

Button M., Moriarty M.M., Watts M.J., Zhang J., Koch I., Reimer K.J. Arsenic speciation in field-collected and laboratory-exposed earthworms Lumbricus terrestris. Chemosphere. 2011;85:1277–1283. doi: 10.1016/j.chemosphere.2011.07.026. PubMed DOI

Sácký J., Leonhardt T., Borovička J., Gryndler M., Briksí A., Kotrba P. Intracellular Sequestration of Zinc, Cadmium and Silver in Hebeloma mesophaeum and Characterization of Its Metallothionein Genes. Fungal Genet. Biol. 2014;67:3–14. doi: 10.1016/j.fgb.2014.03.003. PubMed DOI

Du Z., Bramlage W.J. Modifified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. J. Agric. Food Chem. 1992;40:1566–1570. doi: 10.1021/jf00021a018. DOI

Singleton V.L., Rossi J.A. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 1965;16:144–158. doi: 10.5344/ajev.1965.16.3.144. DOI

Shraim A.M., Ahmed T.A., Rahman M.M., Hijji Y.M. Determination of Total Flavonoid Content by Aluminum Chloride Assay: A Critical Evaluation. LWT. 2021;150:111932. doi: 10.1016/j.lwt.2021.111932. DOI

Szaufer-Hajdrych M. Phenolic acids in leaves of species of the Aquilegia genus. Herba Pol. 2004;50:10–14.

Prieto P., Pineda M., Aguilar M. Spectrophotometric Quantitation of Antioxidant Capacity through the Formation of a Phosphomolybdenum Complex: Specific Application to the Determination of Vitamin E. Anal. Biochem. 1999;269:337–341. doi: 10.1006/abio.1999.4019. PubMed DOI

Smilauer P., Leps J. Multivariate Analysis of Ecological Data Using Canoco 5. Cambridge University Press; Cambridge, UK: 2014.

Saha N., Zaman M.R. Evaluation of possible health risks of heavy metals by consumption of foodstuffs available in the central market of Rajshahi City, Bangladesh. Environ. Monit. Assess. 2013;185:3867–3878. doi: 10.1007/s10661-012-2835-2. PubMed DOI

Dahal B.M., Fuerhacker M., Mentler A., Karki K.B., Shrestha R.R., Blum W.E.H. Arsenic contamination of soils and agricultural plants through irrigation water in Nepal. Environ. Pollut. 2008;155:157–163. doi: 10.1016/j.envpol.2007.10.024. PubMed DOI

Hartley W., Lepp N.W. Remediation of arsenic contaminated soils by iron-oxide application, evaluated in terms of plant productivity, arsenic and phytotoxic metal uptake. Sci. Total Environ. 2008;390:35–44. doi: 10.1016/j.scitotenv.2007.09.021. PubMed DOI

Pavlík M., Pavlíková D., Staszková L., Neuberg M., Kaliszová R., Száková J., Tlustoš P. The effect of arsenic contamination on amino acids metabolism in Spinacia oleracea L. Ecotoxicol. Environ. Saf. 2010;73:1309–1313. doi: 10.1016/j.ecoenv.2010.07.008. PubMed DOI

Meng Y., Zhang L., Yao Z.-L., Ren Y.-B., Wang L.-Q., Ou X.-B. Arsenic accumulation and physiological response of three leafy vegetable varieties to As stress. Int. J. Environ. Res. Public. Health. 2022;19:2501. doi: 10.3390/ijerph19052501. PubMed DOI PMC

Srivastava S., Sharma Y.K. Altered growth, photosynthetic machinery and induced oxidative stress in spinach in response to arsenic stress. J. Plant. Physiol. Pathol. 2013;1:2.

Nihal A., Mithun P.R., Praveen N. Effect of heavy metals (Hg, As and La) on biochemical constituents of Spinacia oleracea. J. Pharmacogn. Phytochem. 2019;8:669–674.

Finnegan P.M., Chen W. Arsenic toxicity: The effects on plant metabolism. Front. Physiol. 2012;6:182. doi: 10.3389/fphys.2012.00182. PubMed DOI PMC

González-Moscoso M., Juárez-Maldonado A., Cadenas-Pliego G., Meza-Figueroa D., SenGupta B., Martínez-Villegas N. Silicon nanoparticles decrease arsenic translocation and mitigate phytotoxicity in tomato plants. Environ. Sci. Pollut. Res. 2022;29:34147–34163. doi: 10.1007/s11356-021-17665-2. PubMed DOI

Keilig K., Ludwig-Mueller J. Effect of flavonoids on heavy metal tolerance in Arabidopsis thaliana seedlings. Bot. Stud. 2009;50:311–318.

Pandey N., Patkak G.C., Pandey D.K., Pandey R. Heavy metals, Co, Ni, Cu, Zn and Cd, produce oxidative damage and evoke differential antioxidant responses in spinach. Braz. J. Plant Physiol. 2009;21:103–111.

Colak N., Torun H., Gruz J., Strnad M., Ayaz F.A. Exogenous N-Acetylcysteine alleviates heavy metal stress by promoting phenolic acids to support antioxidant defence systems in wheat roots. Ecotoxicol. Environ. Saf. 2019;181:49–59. doi: 10.1016/j.ecoenv.2019.05.052. PubMed DOI

Zhao L., Huang Y., Adeleye A.S., Keller A.A. Metabolomics reveals Cu(OH)2 nanopesticide-activated anti-oxidative pathways and decreased beneficial antioxidants in spinach leaves. Environ. Sci. Technol. 2017;51:10184–10194. doi: 10.1021/acs.est.7b02163. PubMed DOI

Wu L., Yi H., Min Y. Assessment of arsenic toxicity using Allium/Vicia root tip micronucleus assays. J. Hazard. Mater. 2010;176:952–956. doi: 10.1016/j.jhazmat.2009.11.132. PubMed DOI

Yi H., Wu L., Jiang L. Genotoxicity of arsenic evaluated by Allium-root micronucleus assay. Sci. Total Environ. 2007;383:232–236. doi: 10.1016/j.scitotenv.2007.05.015. PubMed DOI

Aina R., Sgorbati S., Santagostino A., Labra M., Ghiani A., Citterio S. Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol. Plant. 2004;121:472–480. doi: 10.1111/j.1399-3054.2004.00343.x. DOI

Bolukbasi E. Methylation Modelling and Epigenetic Analysis of Sunflower (Helianthus annuus L.) Seedlings Exposed to Cadmium Heavy Metal Stress. KSU J. Agric. Nat. 2022;25:467–475. doi: 10.18016/ksutarimdoga.vi.883985. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace