SUMMARY. The study of Arabidopsis ecotypes from the Chornobyl area demonstrated their enhanced resistance to cad-mium (Cd2+) and radiomimetics (bleomycin/zeocin). For instance, the seedlings of the Chornobyl ecotype Che07 demonstrated lower inhibition of root growth under Cd-induced stress. It was first determined that zeocin mainly affected the cells of the root meristem, whereas Cd2+ predominantly impacted the cells of the elongation zone. This differentiated response may result from variations in the stages of plant development, the specific action of genotoxic agents, and the activity of protective mechanisms in different growth zones of the roots. The analysis of DNA destruction and its ability to recover after processing with radiomimetics demonstrated the rapid (within three minutes) activation of repair mechanisms in the Chornobyl ecotypes Che5 and Che07. The enhanced expression of the cyclin gene CycB2;1 and poorer expression of the kinase gene CDKG1 after processing with bleomycin indicated the presence of changes in the regulation of the cellular cycle, specifically its arrest in the G2 phase. This adaptive response might be directed at inhibiting the transition to mitosis, which prevents the transfer of the damaged DNA to daughter cells. In Arabidopsis ecotypes from the Chornobyl area, there was activation of the specific antioxidant enzymes, which counteracts the oxidative stress and genome damage. It is assumed that Arabidopsis plants from the area of the Chornobyl nuclear power station employ unique mechanisms of adaptation to ecological stress and DNA damage, which may have been acquired due to the long-term impact of ionizing radiation. The investigation of plant resistance to ionizing radiation and heavy metals is relevant for the elaboration of phytoremediation strategies and may promote the development of biotechnologies to enhance plant resistance to other abiotic stress factors.
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Abramov, V.I., Fedorenko. O., and Shevchenko, V., Genetic consequences of radioactive contaminations for populations of Arabidopsis, Sci. Total Environ., 1992a, vol. 112, pp. 19–28.
Abramov, V.I., Sergeyeva, S.A., Ptitsyna, S.N., Semov, A.B., and Shevchenko, V.A., Genetic-effects and repair of single-stranded-DNA breaks in populations of Arabidopsis thaliana growing in the region of the Chernobyl-nuclear-power-station, Genetika, 1992b, vol. 28, pp. 69–73
Angelis, K.J., Dušinská, M., and Collins, A.R., Single cell gel electrophoresis: detection of DNA damage at different levels of sensitivity, Electrophoresis, 1999, vol. 20, pp. 2133–2138.
Arkhipov, N.P., Kuchma, N.D., Askbrant, S., Pasternak, P.S., and Musica, V.V., Acute and long-term effects of irradiation on pine (Pinus silvestris) stands post-Chernobyl, Sci. Total Environ., 1994, vol. 157, pp. 383–386.
Badia, M.B., Arias, C.L., Tronconi, M.A., Maurino, V.G., Andreo, C.S., Drincovich, M.F., and Wheeler, M.C., Enhanced cytosolic NADP-ME2 activity in A. thaliana affects plant development, stress tolerance and specific diurnal and nocturnal cellular processes, Plant Sci., 2015, vol. 240, pp. 193–203. https://doi.org/10.1016/j.plantsci.2015.09.015
Baluška, F., Mancuso, S., Volkmann, D., and Barlow, P.W., Root apex transition zone: a signalling-response nexus in the root, Trends Plant Sci., 2010, vol. 15, no. 7, pp. 402–408. https://doi.org/10.1016/j.tplants.2010.04.007
Caplin, N. and Willey, N., Ionizing radiation, higher plants, and radioprotection: from acute high doses to chronic low doses, Front. Plant Sci., 2018, vol. 9, p. 847. https://doi.org/10.3389/fpls.2018.00847
Chao, Yu.Ya., Hong, Ch-Ya., and Kao, Ch.H., The decline in ascorbic acid content is associated with cadmium toxicity of rice seedlings, Plant Physiol. Biochem., 2010, vol. 48, no. 5, pp. 374–381. https://doi.org/10.1016/j.plaphy.2010.01.009
Chivasa, S, Tomé, D.F., Hamilton, J.M., and Slabas, A.R., Proteomic analysis of extracellular ATP-regulated proteins identifies ATP synthase beta-subunit as a novel plant cell death regulator, Mol. Cell. Proteomics, 2011, vol. 10, no. 3, p. M110.003905. https://doi.org/10.1074/mcp.M110.003905
Danchenko, M., Skultety, L., Rashydov, N. M., Berezhna, V.V., Mátel, L., Salaj, T., Pretova, A., and Haiduch, M., Proteomic analysis of mature soybean seeds from the Chernobyl area suggests plant adaptation to the contaminated environment, J. Proteome Res., 2009, vol. 8, pp. 2915–2922.
Della Rovere, F., Fattorini, L., Ronzan, M., Falasca, G., and Altamura, M.M., The quiescent center and the stem cell niche in the adventitious roots of Arabidopsis thaliana, Plant Signal. Behav., 2016, vol. 11, p. e1176660. https://doi.org/10.1080/15592324.2016.1176660
Giovannoni, J., Completing a pathway to plant vitamin C synthesis, Proceedings of the Natl. Acad. Sci., vol. 104, no. 22, pp. 9109–9110. https://doi.org/10.1073/pnas.0703222104
Hasanuzzaman, M., Nahar, K., Anee, T.I., and Fujita, M., Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance, Physiol. Mol. Biol. Plants, 2017, vol. 23, no. 2, pp. 249–268. https://doi.org/10.1007/s12298-017-0422-2
Ito, M., Expression of mitotic cyclins in higher plants: transcriptional and proteolytic regulation, Plant Biotechnol. Rep., 2014, vol. 8, p. 9. https://doi.org/10.1007/s11816-013-0297-9
Kim, Y.S., Analysis of gene expression upon DNA damage in Arabidopsis, J. Plant Biol., 2006, vol. 49, pp. 298–302. https://doi.org/10.1007/BF03031159
Klimenko, O., Pernis, M., Danchenko, M., Skultéty, L., Klubicová, K., and Shevchenko, G., Natural ecotype of Arabidopsis thaliana (L.) Heynh (Chernobyl-07) respond to cadmium stress more intensively than the sensitive ecotypes Oasis and Columbia, Ecotoxicol. Environ. Saf., 2019, vol. 173, pp. 86–95. https://doi.org/10.1016/j.ecoenv.2019.02.012
Klubicová, K., Danchenko, M., Skultety, L., Berezhna, V.V., Hricová, A., Rashydov, N. M., and Haiduch M., Agricultural recovery of a formerly radioactive area: II. Systematic proteomic characterization of flax seed development in the remediated Chernobyl area, J. Proteomics, 2011b, vol. 74, pp. 1378–1384.
Kovalchuk, O., Burke, P., Arkhipov, A., Kuchma, N., James, S.J., Kovalchuk, I., and Pogribny, I., Genome hypermethylation in Pinus silvestris of Chernobyl – a mechanism for radiation adaptation?, Mutat. Res., 2003a, vol. 529, pp. 13–20.
Kovalchuk, O., Kovalchuk, I., Arkhipov, A., Hohn, B., and Dubrova, Yu.E., Extremely complex pattern of microsatellite mutation in the germline of wheat exposed to the post-Chernobyl radioactive contamination, Mutat. Res., 2003b, vol. 525, pp. 93–101.
Kovalchuk, I., Abramov, V., Pogribny, I., and Kovalchuk, O., Molecular aspects of plant adaptation to life in the Chernobyl zone, Plant Physiol., 2004, vol. 35, pp. 357–363.
Li, S., Mhamdi, A., Clement, C., Jolivet, Y., and Noctor, G., Analysis of knockout mutants suggests that Arabidopsis NADP-malic enzyme 2 does not play an essential role in responses to oxidative stress of intracellular or extracellular origin, J. Exp. Bot., 2013, vol. 64, pp. 3605–3614.
Lin, J., Yang, K., Zheng, B., and Deng, X., Phosphorylation of Arabidopsis SINA2 by CDKG1 affects its ubiquitin ligase activity and degradation under abiotic stress, BMC Plant Biol., 2018, vol. 18, no. 1, pp. 1–14.
Liu, S., Cheng, Y., Zhang, X., Guan, Q., Nishiuchi, S., Hase, K., and Takano, T., Expression of an NADPmalic enzyme gene in rice (Oryza sativa. L) is induced by environmental stresses; over-expression of the gene in Arabidopsis confers salt and osmotic stress tolerance, Plant Mol. Biol., 2007, vol. 64, pp. 49–58.
Liu, H., Liu, Z., Qin, A., Zhou, Y., Sun, S., Liu, Y., Hu, M., Yang, J., and Sun, X., Mitochondrial ATP synthase beta-subunit affects plastid retrograde signaling in Arabidopsis, Int. J. Mol. Sci., 2024, vol. 25, no. 14, p. 7829. https://doi.org/10.3390/ijms25147829
Ludovici, G.M., de Souza, S.O., Chierici, A., Cascone, M.G., d’Errico, F., and Malizia, A., Adaptation to ionizing radiation of higher plants: From environmental radioactivity to Chernobyl disaster, J. Environ. Radioact., 2020, vol. 222, p. 106375. https://doi.org/10.1016/j.jenvrad.2020.106375
Manova, V. and Gruszka, D., DNA damage and repair in plants – from models to crops, Front. Plant Sci., 2015, vol. 6. https://doi.org/10.3389/fpls.2015.00885
Manova, V., Gecheff, G., and Stoilov, L., Efficient repair of bleomycin-induced double-strand breaks in barley ribosomal genes, Mutat. Res., 2006, vol. 601, nos. 1–2, pp. 179–190. https://doi.org/10.1016/j.mrfmmm.2006.07.004
Nibau, C., Dadarou, D., Kargios, N., Mallioura, A., Fernandez-Fuentes, N., Cavallari, N., and Doonan, J. H., CDKG1 is required for meiotic and somatic recombination intermediate processing in Arabidopsis, Plant Cell, 2020, vol. 32, no. 4, pp. 1308–1322
Podlutskii, M., Babina, D., Podobed, M., Bondarenko, E., Bitarishvili, S., Blinova, Y., Shesterikova, E., Prazyan, A., Turchin, L., Garbaruk. D., Kudin, M., Duarte, G.T., and Volkova, P., Arabidopsis thaliana accessions from the Chernobyl exclusion zone show decreased sensitivity to additional acute irradiation, Plants, 2024, vol. 13, no. 7, p. 947. https://doi.org/10.3390/plants13070947
Rashydov, N. and Hajduch, M., Chernobyl seed project. Advances in the identification of differentially abundant proteins in a radio-contaminated environment, Front. Plant Sci., 2015, vol. 6. https://doi.org/10.3389/fpls.2015.00493
Saruyama, N., Sakakura, Y., Asano, T., Nishiuchi, T., Sasamoto, H., and Kodama, H., Quantification of metabolic activity of cultured plant cells by vital staining with fluorescein diacetate, Anal. Biochem., 2013, vol. 441, no. 1, pp. 58–62. https://doi.org/10.1016/j.ab.2013.06.005
Schnittger, A. and De Veylder L. The dual face of cyclin B1, Trends Plant Sci., 2018, vol 23, no. 6, pp. 475–478.
Shevchenko, G.V. and Talalaiev, O.S., Efficient mechanism of DNA repair stabilizes genome of Arabidopsis thaliana from the Chernobyl zone, Dopov. Nac. Akad. Nauk (Ukr.), 2017, pp. 84–90. https://doi.org/10.15407/dopovidi2017.04.084
Shkvarnikov, P.K., A cytological study of plants growing under exposure to different radiation levels, Tsitol. G-enet., 1990, vol. 24, pp. 33–37.
Szurman-Zubrzycka, M., Jędrzejek, P., and Szarejko, I., How do plants cope with DNA damage? A concise review on the DDR pathway in plants, Int. J. Mol. Sci., 2023, vol. 24, no. 3, p. 2404. https://doi.org/10.3390/ijms24032404
Truernit, E. and Haseloff, J., A simple way to identify non-viable cells within living plant tissue using confocal microscopy, Plant Methods, 2008, vol. 4, p. 15
Vladejić, J., Kovacik, M., Zwyrtková, J., et al., Zeocin-induced DNA damage response in barley and its dependence on ATR, Sci. Rep., 2024, vol. 14, p. 3119. https://doi.org/10.1038/s41598-024-53264-0
Wolucka, B.A. and van Montagu M., GDP-mannose 3,5-epimerase forms GDP-L-gulose, a putative intermediate for the de novo diosynthesis of vitamin C in plants, J. Biol. Chem., 2003, vol. 278, no. 48, pp. 47483–47490. https://doi.org/10.1074/jbc.M309135200
Yu, Q., Tian, H., Yue, K., Liu, J., Zhang, B., Li, X., and Ding, Z., A P-loop NTPase regulates quiescent center cell division and distal stem cell identity through the regulation of ROS homeostasis in Arabidopsis root, PLoS Genet., 2016, vol. 12, p. e1006175. https://doi.org/10.1371/journal.pgen.1006175