Effect of Arsenic Soil Contamination on Stress Response Metabolites, 5-Methylcytosine Level and CDC25 Expression in Spinach
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
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
PubMed
37505533
PubMed Central
PMC10383220
DOI
10.3390/toxics11070568
PII: toxics11070568
Knihovny.cz E-zdroje
- Klíčová slova
- CDC25, arsenic species, epigenetics, membrane damage, secondary metabolites, spinach,
- Publikační typ
- časopisecké články MeSH
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.
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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