دورية أكاديمية
أعرض في EDS

DNA methylation is enhanced during Cd hyperaccumulation in Noccaea caerulescens ecotype Ganges.

التفاصيل البيبلوغرافية
العنوان: DNA methylation is enhanced during Cd hyperaccumulation in Noccaea caerulescens ecotype Ganges.
المؤلفون: Galati S; Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy., DalCorso G; Department of Biotechnology, University of Verona, Verona, Italy., Furini A; Department of Biotechnology, University of Verona, Verona, Italy., Fragni R; SSICA, Experimental Station for the Food Preserving Industry, Parma, Italy., Maccari C; Department of Medicine and Surgery, University of Parma, Parma, Italy., Mozzoni P; Department of Medicine and Surgery, University of Parma, Parma, Italy.; Centre for Research in Toxicology (CERT), University of Parma, Parma, Italy., Giannelli G; Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy., Buschini A; Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy., Visioli G; Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy. giovanna.visioli@unipr.it.
المصدر: Environmental science and pollution research international [Environ Sci Pollut Res Int] 2023 Feb; Vol. 30 (10), pp. 26178-26190. Date of Electronic Publication: 2022 Nov 10.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Springer Country of Publication: Germany NLM ID: 9441769 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1614-7499 (Electronic) Linking ISSN: 09441344 NLM ISO Abbreviation: Environ Sci Pollut Res Int Subsets: MEDLINE
أسماء مطبوعة: Publication: <2013->: Berlin : Springer
Original Publication: Landsberg, Germany : Ecomed
مواضيع طبية MeSH: Arabidopsis*/genetics , Arabidopsis*/metabolism , Brassicaceae*/metabolism , Thlaspi*/genetics , Thlaspi*/metabolism , Arabidopsis Proteins*/genetics, Cadmium/metabolism ; DNA Methylation ; Ecotype ; DNA (Cytosine-5-)-Methyltransferases/genetics ; DNA (Cytosine-5-)-Methyltransferases/metabolism
مستخلص: In this study, we assess the DNA damage occurring in response to cadmium (Cd) in the Cd hyperaccumulator Noccaea caerulescens Ganges (GA) vs the non-accumulator and close-relative species Arabidopsis thaliana. At this purpose, the alkaline comet assay was utilized to evaluate the Cd-induced variations in nucleoids and the methy-sens comet assay, and semiquantitative real-time (qRT)-PCR were also performed to associate nucleus variations to possible DNA modifications. Cadmium induced high DNA damages in nuclei of A. thaliana while only a small increase in DNA migration was observed in N. caerulescens GA. In addition, in N. caerulescens GA, CpG DNA methylation increase upon Cd when compared to control condition, along with an increase in the expression of MET1 gene, coding for the DNA-methyltransferase. N. caerulescens GA does not show any oxidative stress under Cd treatment, while A. thaliana Cd-treated plants showed an upregulation of transcripts of the respiratory burst oxidase, accumulation of reactive oxygen species, and enhanced superoxide dismutase activity. These data suggest that epigenetic modifications occur in the N. caerulescens GA exposed to Cd to preserve genome integrity, contributing to Cd tolerance.
(© 2022. The Author(s).)
References: Aina R, Sgorbati S, Santagostino A, Labra M, Ghiani A, Citterio S (2004) Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol Plant 121:472–480. https://doi.org/10.1111/j.1399-3054.2004.00343.x. (PMID: 10.1111/j.1399-3054.2004.00343.x)
Akhter Z, Bi Z, Ali K, Sun C, Fiaz S, Haider FU, Bai J (2021) In response to abiotic Stress, DNA methylation confers epiGenetic changes in plants. Plants 10(6):1096. https://doi.org/10.3390/plants10061096. (PMID: 10.3390/plants10061096)
Assuncão AGL, Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419. https://doi.org/10.1046/j.1469-8137.2003.00819.x. (PMID: 10.1046/j.1469-8137.2003.00819.x)
Bannenberg G, Martínez M, Hamberg M, Castresana C (2009) Diversity of the enzymatic activity in the lipoxygenase gene family of Arabidopsis thaliana. Lipids 44(2):85–95. https://doi.org/10.1007/s11745-008-3245-7. (PMID: 10.1007/s11745-008-3245-7)
Cao X, Jacobsen SE (2002) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12:1138–1144. https://doi.org/10.1016/S0960-9822(02)00925-9. (PMID: 10.1016/S0960-9822(02)00925-9)
Chen RZ, Pettersson U, Beard C, Jackson-Grusby L, Jaenisch R (1998) DNA hypomethylation leads to elevated mutation rates. Nature 395(6697):89–93. https://doi.org/10.1038/25779. (PMID: 10.1038/25779)
Chiorcea-Paquim AM (2022) 8-oxoguanine and 8-oxodeoxyguanosine biomarkers of oxidative DNA damage: a review on HPLC–ECD determination. Molecules 27(5):1620. https://doi.org/10.3390/molecules27051620. (PMID: 10.3390/molecules27051620)
Chu CC, Lee WC, Guo WY, Pan SM, Chen LJ, Li HM, Jinn TL (2005) A copper chaperone for superoxide dismutase that confers three types of copper/zinc superoxide dismutase activity in Arabidopsis. Plant Physiol 139(1):425–36. https://doi.org/10.1104/pp.105.065284.
Connolly EL, Fett JP, Guerinot ML (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14(6):1347–1357. https://doi.org/10.1105/tpc.001263. (PMID: 10.1105/tpc.001263)
Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H, Opdenakker K, Nair AR, Munters E, Artois TJ et al (2010) Cadmium stress: An oxidative challenge. Biometals 23:927–940. https://doi.org/10.1007/s10534-010-9329-x. (PMID: 10.1007/s10534-010-9329-x)
De Caroli M, Furini A, DalCorso G, Rojas M, Di Sansebastiano GP (2020) Endomembrane reorganization induced by heavy metals. Plants 9:482. https://doi.org/10.3390/plants9040482. (PMID: 10.3390/plants9040482)
Drazkiewicz M, Skorzynska-Polit E, Krupa Z (2007) The redox state and activity of superoxide dismutase classes in Arabidopsis thaliana under cadmium or copper stress. Chemosphere 67:188–193. https://doi.org/10.1016/j.chemosphere.2006.08.032. (PMID: 10.1016/j.chemosphere.2006.08.032)
Dutta S, Mitra M, Agarwal P, Mahapatra K, De S, Sett U, Roy S (2018) Oxidative and genotoxic damages in plants in response to heavy metal stress and maintenance of genome stability. Plant Signal Behav 13(8):e1460048. https://doi.org/10.1080/15592324.2018.1460048. (PMID: 10.1080/15592324.2018.1460048)
Fan SK, Ye JY, Zhang LL, Chen HS, Zhang HH, Zhu YX, Liu XX, Jin CW (2020) Inhibition of DNA demethylation enhances plant tolerance to cadmium toxicity by improving iron nutrition. Plant Cell Environ 43:275–291. https://doi.org/10.1111/pce.13670. (PMID: 10.1111/pce.13670)
Feng SJ, Liu XS, Tao H, Tan SK, Chu SS, Oono Y, Zhang XD, Chen J, Yang ZM (2016) Variation of DNA methylation patterns associated with gene expression in rice (Oryza sativa) exposed to cadmium. Plant Cell Environ 39:2629–2649. https://doi.org/10.1111/pce.12793. (PMID: 10.1111/pce.12793)
Galati S, Gullì M, Giannelli G, Furini A, DalCorso G, Fragni R, Buschini A, Visioli G (2021) Heavy metals modulate DNA compaction and methylation at CpG sites in the metal hyperaccumulator Arabidopsis halleri. Environ Mol Mutagen 62(2):133–142. https://doi.org/10.1002/em.22421. (PMID: 10.1002/em.22421)
Guan MY, Zhang HH, Pan W, Jin CW, Lin XY (2018) Sulfide alleviates cadmium toxicity in Arabidopsis plants by altering the chemical form and the subcellular distribution of cadmium. Sci Total Environ 627:663–670. https://doi.org/10.1016/j.scitotenv.2018.01.245. (PMID: 10.1016/j.scitotenv.2018.01.245)
Gullì M, Marchi L, Fragni R, Buschini A, Visioli G (2018) Epigenetic modifications preserve the hyperaccumulator Noccaea caerulescens from Ni geno-toxicity. Environ Mol Mutag 59(6):464–475. https://doi.org/10.1002/em.22191.
Gupta DK, Pena LB, Romero-Puertas MC, Hernández A, Inouhe M, Sandalio LM (2017) NADPH oxidases differentially regulate ROS metabolism and nutrient uptake under cadmium toxicity. Plant Cell Environ 40(4):509–526. https://doi.org/10.1111/pce.12711. (PMID: 10.1111/pce.12711)
Haider FU, Liqun C, Coulter JA, Cheema SA, Wu J, Zhang R, Wenjun M, Farooq M (2021) Cadmium toxicity in plants: impacts and remediation strategies. Ecotoxicol Environ Saf 211:111887. https://doi.org/10.1016/j.ecoenv.2020.111887. (PMID: 10.1016/j.ecoenv.2020.111887)
Halimaa P, Blande D, Baltzi E, Aarts MGM, Granlund L, Keinänen M, Kärenlampi SO, Kozhevnikova AD, Peräniemi S, Schat H, Seregin IV, Tuomainen M, Tervahauta AI (2019) Transcriptional effects of cadmium on iron homeostasis differ in calamine accessions of Noccaea caerulescens. Plant J 97:306–320. https://doi.org/10.1111/tpj.14121. (PMID: 10.1111/tpj.14121)
Holubek R, Deckert J, Zinicovscaia I, Yushin N, Vergel K, Frontasyeva M, Sirotkin AV, Bajia DS, Chmielowska-Bąk J (2020) The recovery of soybean plants after short-term cadmium stress. Plants 9(6):782. https://doi.org/10.3390/plants9060782.
Howe GA, Schilmiller AL (2002) Oxylipin metabolism in response to stress. Curr Opin Plant Biol 5(3):230–236. https://doi.org/10.1016/s1369-5266(02)00250-9. (PMID: 10.1016/s1369-5266(02)00250-9)
Huang H, Ullah F, Zhou DX, Yi M, Zhao Y (2019) Mechanisms of ROS regulation of plant development and stress responses. Front Plant Sci 25(10):800. https://doi.org/10.3389/fpls.2019.00800. (PMID: 10.3389/fpls.2019.00800.PMID:31293607;PMCID:PMC6603150)
Huang X, Duan S, Wu Q, Yu M, Shabala S (2020) Reducing cadmium accumulation in plants: structure–function relations and tissue-specific operation of transporters in the spotlight. Plants 9:223. https://doi.org/10.3390/plants9020223. (PMID: 10.3390/plants9020223)
Jeddeloh JA, Stokes TL, Richards EJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22:94–97. https://doi.org/10.1038/8803. (PMID: 10.1038/8803)
Jing M, Zhang H, Wei M, Tang Y, Xia Y, Chen Y, Shen Z, Chen C (2022) Reactive oxygen species partly mediate DNA methylation in responses to different heavy metals in pokeweed. Front Plant Sci 13:845108. https://doi.org/10.3389/fpls.2022.845108. (PMID: 10.3389/fpls.2022.845108)
Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283:65–87. https://doi.org/10.1016/j.tox.2011.03.001. (PMID: 10.1016/j.tox.2011.03.001)
Junglee S, Urban L, Sallanon H, Lopez-Lauri F (2014) Optimized assay for hydrogen peroxide determination in plant tissue using potassium iodide. Am J Anal Chem 5:730–736. https://doi.org/10.4236/ajac.2014.511081. (PMID: 10.4236/ajac.2014.511081)
Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, Jeddeloh JA, Riddle NC, Verbsky ML, Richards EJ (2003) Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163:1109–1122. https://doi.org/10.1093/genetics/163.3.1109. (PMID: 10.1093/genetics/163.3.1109)
Keunen E, Remans T, Opdenakker K, Jozefczak M, Gielen H, Guisez Y, Vangronsveld J, Cuypers A (2013) A mutant of the Arabidopsis thaliana LIPOXYGENASE1 gene shows altered signalling and oxidative stress related responses after cadmium exposure. Plant Physiol Biochem 63:272–280. https://doi.org/10.1016/j.plaphy.2012.12.005. (PMID: 10.1016/j.plaphy.2012.12.005)
Lane TW, Saito MA, George GN, Pickering IJ, Prince RC, Morel FFM (2005) A cadmium enzyme from a marine diatom. Nature 435:42. https://doi.org/10.1038/435042a. (PMID: 10.1038/435042a)
Li Z, Han X, Song X, Zhang Y, Jiang J, Han Q, Liu M, Qiao G, Zhuo R (2017) Overexpressing the Sedum alfredii Cu/Zn superoxide dismutase increased resistance to oxidative stress in transgenic arabidopsis. Front Plant Sci 8:1010. https://doi.org/10.3389/fpls.2017.01010. (PMID: 10.3389/fpls.2017.01010)
Liu J, He Z (2020) Small DNA methylation, big player in plant abiotic stress responses and memory. Front Plant Sci 11:595603. https://doi.org/10.3389/fpls.2020.595603. (PMID: 10.3389/fpls.2020.595603)
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262.
López MA, Vicente J, Kulasekaran S, Vellosillo T, Martínez M, Irigoyen ML, Cascón T, Bannenberg G, Hamberg M, Castresana C (2011) Antagonistic role of 9-lipoxygenase-derived oxylipins and ethylene in the control of oxidative stress, lipid peroxidation and plant defence. Plant J 67(3):447–458. https://doi.org/10.1111/j.1365-313X.2011.04608.x. (PMID: 10.1111/j.1365-313X.2011.04608.x)
Manara A, Fasani E, Furini A, DalCorso G (2020) Evolution of the metal hyperaccumulation and hypertolerance traits. Plant Cell Environ 43(12):2969–2986. https://doi.org/10.1111/pce.13821. (PMID: 10.1111/pce.13821)
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497. (PMID: 10.1111/j.1399-3054.1962.tb08052.x)
Niekerk L-A, Carelse MF, Bakare OO, Mavumengwana V, Keyster M, Gokul A (2021) The Relationship between Cadmium Toxicity and the Modulation of Epigenetic Traits in Plants. Int J Mol Sci 22:7046. https://doi.org/10.3390/ijms22137046. (PMID: 10.3390/ijms22137046)
Ou X, Zhang Y, Xu C, Lin X, Zang Q, Zhuang T, Jiang L, von Wettstein D, Liu B (2012) Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in rice (Oryza sativa L.). PLoS ONE 7:e41143. https://doi.org/10.1371/journal.pone.0041143. (PMID: 10.1371/journal.pone.0041143)
Perotti A, Rossi V, Mutti A, Buschini A (2015) Methy-sens comet assay and DNMTs transcriptional analysis as a combined approach in epigenotoxicology. Biomarkers 20(1):64–70. https://doi.org/10.3109/1354750X.2014.992813. (PMID: 10.3109/1354750X.2014.992813)
Pizzaia D, Nogueira ML, Mondin M, Carvalho MEA, Piotto FA, Rosario MF, Azevedo RA (2019) Cadmium toxicity and its relationship with disturbances in the cytoskeleton, cell cycle and chromosome stability. Ecotoxicology 28(9):1046–1055. https://doi.org/10.1007/s10646-019-02096-0. (PMID: 10.1007/s10646-019-02096-0)
Rao MV, Davis KR (1999) Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J 17:603–614. https://doi.org/10.1046/j.1365-313X.1999.00400.x.
Reeves RD, Baker AJM, Jaffré T, Erskine PD, Echevarria G, van der Ent A (2018) A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol 218(2):407–411. https://doi.org/10.1111/nph.14907. (PMID: 10.1111/nph.14907)
Rodriguez E, Sousa M, Gomes A, Azevedo R, Mariz-Ponte N, Sario S, Mendes RJ, Santos C (2019) Genotoxic endpoints in a Pb-accumulating pea cultivar: insights into Pb2+ contamination limits. Environ Sci Pollut Res Int 26(31):32368–32373. https://doi.org/10.1007/s11356-019-06465-4. (PMID: 10.1007/s11356-019-06465-4)
Romero-Puertas MC, Corpas FJ, Rodriguez-Serrano M, Gomez M, del Río LA, Sandalio LM (2007) Differential expression and regulation of antioxidative enzymes by Cd in pea plants. J Plant Physiol 164(10):1346–1357. https://doi.org/10.1016/j.jplph.2006.06.018. (PMID: 10.1016/j.jplph.2006.06.018)
Sebastian A, Prasad MNV (2018) Exogenous citrate and malate alleviate cadmium stress in Oryza sativa L.: Probing role of cadmium localization and iron nutrition. Ecotoxicol Environ Saf 166:215–222. https://doi.org/10.1016/j.ecoenv.2018.09.084. (PMID: 10.1016/j.ecoenv.2018.09.084)
Seth CS, Misra V, Chauhan LK, Singh RR (2008) Genotoxicity of cadmium on root meristem cells of Allium cepa: cytogenetic and Comet assay approach. Ecotoxicol Environ Saf 71(3):711–716. https://doi.org/10.1016/j.ecoenv.2008.02.003. (PMID: 10.1016/j.ecoenv.2008.02.003)
Shafiq S, Zeb Q, Ali A, Sajjad Y, Nazir R, Widemann E, Liu L (2019) Lead, Cadmium and Zinc phytotoxicity alter DNA methylation levels to confer heavy metal tolerance in Wheat. Int J Mol Sci 20:4676. https://doi.org/10.3390/ijms20194676. (PMID: 10.3390/ijms20194676)
Shen Y, Issakidis-Bourguet E, Zhou DX (2016) Perspectives on the interactions between metabolism, redox, and epigenetics in plants. J Exp Bot 67(18):5291–5300. https://doi.org/10.1093/jxb/erw310. (PMID: 10.1093/jxb/erw310)
Shi D, Zhuang K, Xia Y, Zhu C, Chen C, Hu Z et al (2017) Hydrilla verticillata employs two different ways to affect DNA methylation under excess copper stress. Aquat Toxicol 193:97–104. https://doi.org/10.1016/j.aquatox.2017.10.007. (PMID: 10.1016/j.aquatox.2017.10.007)
Singh D, Chaudhary P, Taunk J, Kumar Singh C, Sharma S, Singh VJ, Singh D, Chinnusamy V, Yadav R, Pal M (2021) Plant epigenomics for extenuation of abiotic stresses: challenges and future perspectives. J Exp Bot 72(20):6836–6855. https://doi.org/10.1093/jxb/erab337. (PMID: 10.1093/jxb/erab337)
Skórzyńska-Polit E, Pawlikowska-Pawlęga B, Szczuka E et al (2006) The Activity and Localization of Lipoxygenases in Arabidopsis thaliana under Cadmium and Copper Stresses. Plant Growth Regul 48:29–39. https://doi.org/10.1007/s10725-005-4745-6. (PMID: 10.1007/s10725-005-4745-6)
Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu J-C, Sasaki YF (2000) Single cell gel/Comet assay: Guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35:206–221. https://doi.org/10.1002/(sici)1098-2280(2000)35:3%3c206::aid-em8%3e3.0.co;2-j. (PMID: 10.1002/(sici)1098-2280(2000)35:3<206::aid-em8>3.0.co;2-j)
Valavanidis A, Vlachogianni T, Fiotakis C (2009) 8-hydroxy-2′ -deoxyguanosine (8-OHdG): a critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C 27(2):120–139. https://doi.org/10.1080/10590500902885684. (PMID: 10.1080/10590500902885684)
Wang H, He L, Song J, Cui W, Zhang Y, Jia C, Francis D, Rogers HJ, Sun L, Tai P et al (2016) Cadmium-induced genomic instability in Arabidopsis: molecular toxicological biomarkers for early diagnosis of cadmium stress. Chemosphere 150:258–265. https://doi.org/10.1016/j.chemosphere.2016.02.042. (PMID: 10.1016/j.chemosphere.2016.02.042)
معلومات مُعتمدة: Local Funding for Research University of Parma
فهرسة مساهمة: Keywords: Antioxidant activity; Cadmium toxicity; Comet assay; Epigenetic regulation; Hyperaccumulators; Methy-sens comet assay; Noccaea caerulescens
المشرفين على المادة: 00BH33GNGH (Cadmium)
EC 2.1.1.- (MET1 protein, Arabidopsis)
EC 2.1.1.37 (DNA (Cytosine-5-)-Methyltransferases)
0 (Arabidopsis Proteins)
تواريخ الأحداث: Date Created: 20221109 Date Completed: 20230310 Latest Revision: 20240117
رمز التحديث: 20240117
مُعرف محوري في PubMed: PMC9995422
DOI: 10.1007/s11356-022-23983-w
PMID: 36352075
قاعدة البيانات: MEDLINE
الوصف
تدمد:1614-7499
DOI:10.1007/s11356-022-23983-w