BACKGROUND: Arsenic toxicity induces a range of metabolic responses in plants, including DNA methylation. The focus of this paper was on the relationship between As-induced stress and plant senescence in the hyperaccumulator Pteris cretica var. Albo-lineata (Pc-Al). We assume difference in physiological parameters and level of DNA methylation in young and old fronds as symptoms of As toxicity. RESULTS: The As accumulation of Pc-Al fronds, grown in pots of haplic chernozem contaminated with 100 mg As kg- 1 for 122 days, decreased with age. Content of As was higher in young than old fronds for variants with 100 mg As kg- 1 (2800 and 2000 mg As kg- 1 dry matter, respectively). The highest As content was determined in old fronds of Pc-Al grown in pots with 250 mg As kg- 1. The increase with age was confirmed for determined nutrients - Cu, Mg, Mn, S and Zn. A significant elevation of all analysed nutrients was showed in old fronds. Arsenic accumulation affected DNA methylation status in fronds, but content of 5-methylcytosine (5mC) decreased only in old fronds of Pc-Al (from 25 to 12%). Determined photosynthetic processes showed a decrease of fluorescence, photosynthetic rate and chlorophylls of As treatments in young and old fronds. Water potential was decreased by As in both fronds. Thinning of the sclerenchymatous inner cortex and a reduction in average tracheid metaxylem in the vascular cylinder was showed in roots of As treatment. Irrespective to fronds age, physiological parameters positively correlated with a 5mC while negatively with direct As toxicity. Opposite results were found for contents of Cu, Mg, Mn, S and Zn. CONCLUSIONS: The results of this paper point to changes in the metabolism of the hyperaccumulator plant Pc-Al, upon low and high exposure to As contamination. The significant impact of As on DNA methylation was found in old fronds. Irrespective to fronds age, significant correlations were confirmed for 5mC and As toxicity. Our analysis of the very low water potential values and lignification of cell walls in roots showed that transports of assimilated metabolites and water between roots and fronds were reduced. As was showed by our results, epigenetic changes could affect studied parameters of the As hyperaccumulator plant Pc-Al, especially in old fronds.

Department of Agro Environmental Chemistry and Plant Nutrition Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamýcká 129 16500 Prague Czech Republic

Department of Biochemistry and Microbiology University of Chemistry and Technology Technická 5 16628 Prague Czech Republic

Department of Botany and Plant Physiology Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamýcká 129 16500 Prague Czech Republic

Isotope Laboratory Institute of Experimental Botany The Czech Academy of Sciences Vídeňská 1083 14220 Prague Czech Republic

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Eisler R. Eisler’s encyclopedia of environmentally hazardous priority chemicals. Amsterdam: Elsevier; 2007.

Ye WL, Wood BA, Stroud JL, Andralojc PJ, Raab A, McGrath SP, et al. Arsenic speciation in phloem and xylem exudates of castor bean. Plant Physiol. 2010;154(3):1505–1513. doi: 10.1104/pp.110.163261. PubMed DOI PMC

Zhao FJ, Dunham SJ, McGrath SP. Arsenic hyperaccumulation by different fern species. New Phytol. 2002;156(1):27–31. doi: 10.1046/j.1469-8137.2002.00493.x. DOI

Su YH, McGrath SP, Zhu YG, Zhao FJ. Highly efficient xylem transport of arsenite in the arsenic hyperaccumulator Pteris vittata. New Phytol. 2008;180(2):434–441. doi: 10.1111/j.1469-8137.2008.02584.x. PubMed DOI

Tu C, Ma LQ. Effects of arsenic on concentration and distribution of nutrients in the fronds of the arsenic hyperaccumulator Pteris vittata L. Environ Pollut. 2005;135(2):333–340. doi: 10.1016/j.envpol.2004.03.026. PubMed DOI

Koller CE, Patrick JW, Rose RJ, Offler CE, MacFarlane GR. Pteris umbrosa R. Br. As an arsenic hyperaccumulator: accumulation, partitioning and comparison with the established as hyperaccumulator Pteris vittata. Chemosphere. 2007;66(7):1256–1263. doi: 10.1016/j.chemosphere.2006.07.029. PubMed DOI

Abbas G, Murtaza B, Bibi I, Shahid M, Niazi NK, Khan MI, et al. Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. Int J Environ Res Public Health. 2018;15(1):59. doi: 10.3390/ijerph15010059. PubMed DOI PMC

Agnihotri A, Seth CS. Exogenously applied nitrate improves the photosynthetic performance and nitrogen metabolism in tomato (Solanum lycopersicum L. cv Pusa Rohini) under arsenic (V) toxicity. Physiol Mol Biol Plants. 2016;22(3):341–349. doi: 10.1007/s12298-016-0370-2. PubMed DOI PMC

Foyer CH, Noctor G. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal. 2009;11(4):861–905. doi: 10.1089/ars.2008.2177. PubMed DOI

Yaish MW. Editorial: epigenetic modifications associated with abiotic and biotic stresses in plants: an implication for understanding plant evolution. Front Plant Sci. 2017;8:1983. doi: 10.3389/fpls.2017.01983. PubMed DOI PMC

Lechat MM, Brun G, Montiel G, Véronési C, Simier P, Thoiron S, et al. 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(11):3129–3140. doi: 10.1093/jxb/erv119. PubMed DOI PMC

Bossdorf O, Arcuri D, Richards CL, Pigliucci M. Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana. Evol Ecol. 2010;24(3):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(1):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(2):503–512. doi: 10.1007/s11738-013-1431-6. DOI

Bona E, Cattaneo C, Cesaro P, Marsano F, Lingua G, Cavaletto M, et al. Proteomic analysis of Pteris vittata fronds: two arbuscular mycorrhizal fungi differentially modulate protein expression under arsenic contamination. Proteomics. 2010;10(21):3811–3834. doi: 10.1002/pmic.200900436. PubMed DOI

Campos NV, Araújo TO. Arcanjo-Silva S, Freitas-Silva L, Azevedo AA, Nunes-Nesi A. Arsenic hyperaccumulation induces metabolic reprogramming in Pityrogramma calomelanos to reduce oxidative stress. Physiol Plant. 2016;157(2):135–146. doi: 10.1111/ppl.12426. PubMed DOI

He S, Hu Y, Wang H, Wang H, Li Q. Effects of indole-3-acetic acid on arsenic uptake ad antioxidative enzymes in Pteris cretica var. nervosa and Pteris ensiformis. Int J Phytoremediat. 2017;19(3):231–238. doi: 10.1080/15226514.2016.1207609. PubMed DOI

Nagajyoti PC, Lee KD, Sreekanth TVM. Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett. 2010;8(3):199–216. doi: 10.1007/s10311-010-0297-8. DOI

Ushijima T, Okochi-Takada E. Aberrant methylations in cancer cells: where do they come from? Cancer Sci. 2005;96(4):206–211. doi: 10.1111/j.1349-7006.2005.00035.x. PubMed DOI PMC

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(3):472–480. doi: 10.1111/j.1399-3054.2004.00343.x. DOI

Erturk FA, Aydin M, Sigmaz B, Taspinar MS, Arslan E, Agar G, et al. Effects of As2O3 on DNA methylation, genomic instability, and LTR retrotransposon polymorphism in Zea mays. Environ Sci Pollut Res. 2015;22(23):18601–18606. doi: 10.1007/s11356-015-5426-2. PubMed DOI

Shen H, He H, Li J, Chen W, Wang X, Guo L, et al. Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell. 2012;24(3):875–892. doi: 10.1105/tpc.111.094870. PubMed DOI PMC

Burn JE, Bagnall DJ, Metzger JD, Dennis ES, Peacock WJ. DNA methylation, vernalization, and the initiation of flowering. Proc Natl Acad Sci U S A. 1993;90(1):287–291. doi: 10.1073/pnas.90.1.287. PubMed DOI PMC

Albrechtová JTP, Ullmann J, Krekule J, Seidlová F. Effect of 5-azacytidine on growth pattern in Chenopodium rubrum. Plant Sci. 1994;96(1–2):211–215. doi: 10.1016/0168-9452(94)90238-0. DOI

Arase S, Kasai M, Kanazawa A. In planta assays involving epigenetically silenced genes reveal inhibition of cytosine methylation by genistein. Plant Methods. 2012;8:10. doi: 10.1186/1746-4811-8-10. PubMed DOI PMC

Cazzonelli CI. Carotenoids in nature: insights from plants and beyond. Funct Plant Biol. 2011;38(11):833–847. doi: 10.1071/FP11192. PubMed DOI

Zhang C, Zhang W, Ren G, Li D, Cahoon RE, Chen M, et al. Chlorophyll synthase under epigenetic surveillance is critical for vitamin E synthesis, and altered expression affects tocopherol levels in Arabidopsis. Plant Physiol. 2015;168(4):1503–1511. doi: 10.1104/pp.15.00594. PubMed DOI PMC

Lushchak VI, Semchuk NM. Tocopherol biosynthesis: chemistry, regulation and effects of environmental factors. Acta Physiol Plant. 2012;34(5):1607–1628. doi: 10.1007/s11738-012-0988-9. DOI

Farooq MA, Gill RA, Ali B, Wang J, Islam F, Ali S, et al. Subcellular distribution, modulation of antioxidant and stress-related genes response to arsenic in Brassica napus L. Ecotoxicology. 2016;25(2):350–366. doi: 10.1007/s10646-015-1594-6. PubMed DOI

Wang HB, Xie F, Yao YZ, Zhao B, Xiao QQ, Pan YH, et al. The effects of arsenic and induced-phytoextraction methods on photosynthesis in Pteris species with different arsenic-accumulating abilities. Environ Exp Bot. 2012;75:298–306. doi: 10.1016/j.envexpbot.2011.08.002. DOI

Gaufichon L, Reisdorf-Cren M, Rothstein SJ, Chardon F, Suzuki A. Biological functions of asparagine synthetase in plants. Plant Sci. 2010;179(3):141–153. doi: 10.1016/j.plantsci.2010.04.010. DOI

Ay N, Janack B, Humbeck K. Epigenetic control of plant senescence and linked processes. J Exp Bot. 2014;65(14):3875–3887. doi: 10.1093/jxb/eru132. PubMed DOI

Cakmak I. Tansley review no. 111. Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol. 2000;146(2):185–205. doi: 10.1046/j.1469-8137.2000.00630.x. PubMed DOI

Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Carreras A, Valderrama R, et al. Functional analysis of superoxide dismutases (SODs) in sunflower under biotic and abiotic stress conditions. Identification of two new genes of mitochondrial Mn-SOD. J Plant Physiol. 2011;168(11):1303–1308. doi: 10.1016/j.jplph.2011.01.020. PubMed DOI

Zemanová V, Pavlík M, Pavlíková D. Cadmium toxicity induced contrasting patterns of concentrations of free sarcosine, specific amino acids and selected microelements in two Noccaea species. PLoS One. 2017;12(5):e0177963. doi: 10.1371/journal.pone.0177963. PubMed DOI PMC

Raab A, Feldmann J, Meharg AA. The nature of arsenic-phytochelatin complexes in Holcus lanatus and Pteris cretica. Plant Physiol. 2004;134(3):1113–1122. doi: 10.1104/pp.103.033506. PubMed DOI PMC

Hare PD, Cress WA. Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul. 1997;21(2):79–102. doi: 10.1023/A:1005703923347. DOI

Yamaguchi M, Valliyodan B, Zhang J, Lenoble ME, Yu O, Rogers EE, et al. Regulation of growth response to water stress in the soybean primary root. I. Proteomic analysis reveals region-specific regulation of phenylpropanoid metabolism and control of free iron in the elongation zone. Plant Cell Environ. 2010;33(2):223–243. doi: 10.1111/j.1365-3040.2009.02073.x. PubMed DOI

Smirnoff N. The function and metabolism of ascorbic acid in plants. Ann Bot. 1996;78(6):661–669. doi: 10.1006/anbo.1996.0175. DOI

Abbasi AR, Hajirezaei M, Hofius D, Sonnewald U, Voll LM. Specific roles of α- and γ-tocopherol in abiotic stress responses of transgenic tobacco. Plant Physiol. 2007;143(4):1720–1738. doi: 10.1104/pp.106.094771. PubMed DOI PMC

Tang YL, Ren WW, Zhang L, Tang KX. Molecular cloning and characterization of gene coding for γ-tocopherol methyltransferase from lettuce (Lactuca sativa) Genet Mol Res. 2011;10(4):3204–3212. doi: 10.4238/2011.December.21.2. PubMed DOI

Anterola AM, Lewis NG. Trends in lignin modification: a comprehensive analysis of the effects of genetic manipulations/mutations on lignification and vascular integrity. Phytochemistry. 2002;61(3):221–294. doi: 10.1016/S0031-9422(02)00211-X. PubMed DOI

Gas-Pascual E, Simonovik B, Schaller H, Bach TJ. Inhibition of cycloartenol synthase (CAS) function in tobacco BY-2 cells. Lipids. 2015;50(8):761–772. doi: 10.1007/s11745-015-4036-6. PubMed DOI

Zanella L, Fattorini L, Brunetti P, Roccotiello E, Cornara L, D'Angeli S, et al. Overexpression of AtPCS1 in tobacco increases arsenic and arsenic plus cadmium accumulation and detoxification. Planta. 2016;243(3):605–622. doi: 10.1007/s00425-015-2428-8. PubMed DOI PMC

Piršelová B, Kuna R, Libantová J, Moravčíková J, Matušíková I. Biochemical and physiological comparison of heavy metal-triggered defense responses in the monocot maize and dicot soybean roots. Mol Biol Rep. 2011;38(5):3437–3446. doi: 10.1007/s11033-010-0453-z. PubMed DOI

Zemanová V, Pavlík M, Pavlíková D, Hnilička F, Vondráčková S. Responses to cd stress in two Noccaea species (Noccaea praecox and Noccaea caerulescens) originating from two contaminated sites in Mežica, Slovenia and Redlschlag. Austria Arch Environ Contam Toxicol. 2016;70(3):464–474. doi: 10.1007/s00244-015-0198-8. PubMed DOI

Holá D, Benešová M, Fischer L, Haisel D, Hnilička F, Hniličková H, et al. The disadvantages of being a hybrid during drought: a combined analysis of plant morphology, physiology and leaf proteome in maize. PLoS One. 2017;12(4):e0176121. doi: 10.1371/journal.pone.0176121. PubMed DOI PMC

ter Braak CJF, Šmilauer P. CANOCO reference manual and CanoDraw for windows user’s guide: software for canonical community ordination (version 4.5) Ithaca: Microcomputer Power; 2002.

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