Adaptation to ionizing radiation of higher plants: From environmental radioactivity to chernobyl disaster

Abe, 2005, Arabidopsis RAD51C gene is important for homologous recombination in meiosis and mitosis, Plant Physiol., 139, 896, 10.1104/pp.105.065243 Abramov, 2006, Genetic effects in plant populations in the zone of the Chernobyl accident, Radiats. Biol. Radioecol., 46, 259 Amiro, 1986, Effect of gamma-radiation dose rate and total dose on stem growth of Pinus banksiana (Jack pine) seedlings, Environ. Exp. Bot., 26, 253, 10.1016/0098-8472(86)90037-7 Baverstock, 2006, The Chernobyl accident 20 years on: an assessment of the health consequences and the international response, Environ. Health Perspect., 114, 1312, 10.1289/ehp.9113 Belfield, 2012, Genome-wide analysis of mutations in mutant lineages selected following fast-neutron irradiation mutagenesis of Arabidopsis thaliana, Genome Res., 22, 1306, 10.1101/gr.131474.111 Beresford, 2020, Field effects studies in the Chernobyl exclusion zone: lessons to be learnt, J. Environ. Radioact., 211, 10.1016/j.jenvrad.2019.01.005 Berrin, 2005, Stress induces the expression of AtNADK-1, a gene encoding a NAD (H) kinase in Arabidopsis thaliana, Mol. Genet. Genom., 273, 10, 10.1007/s00438-005-1113-1 Biancotto, 2020, Analysis of a dirty bomb attack in a large metropolitan area: simulate the dispersion of radioactive materials, J. Instrum., 15, 10.1088/1748-0221/15/02/P02019 Bienert, 2006, Membrane transport of hydrogen peroxide, Biochim. Biophys. Acta, 1758, 994, 10.1016/j.bbamem.2006.02.015 Boavida, 2007, Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana, Plant J., 52, 570, 10.1111/j.1365-313X.2007.03248.x Bonisoli-Alquati, 2010, DNA damage in barn swallows (Hirundo rustica) from the Chernobyl region detected by use of the comet assay, Comp. Biochem. Physiol. C Toxicol. Pharmacol., 151, 271, 10.1016/j.cbpc.2009.11.006 Bostrack, 1970, The radiosensitivity of gymnosperms II. On the nature of radiation injury and cause of death of Pinus rigida and P. strobus after chronic gamma irradiation, Radiat. Bot., 10, 131, 10.1016/S0033-7560(70)80034-5 Boubriak, 2016, Long term effects of Chernobyl contamination on DNA repair function and plant resistance to different biotic and abiotic stress factors, Cytol. Genet., 50, 381, 10.3103/S0095452716060049 Boyko, 2011, Genetic and epigenetic effects of plant–pathogen interactions: an evolutionary perspective, Mol. Plant, 4, 1014, 10.1093/mp/ssr022 Byrne, 2014, Evolution of extreme resistance to ionizing radiation via genetic adaptation of DNA repair, Elife, 3, 10.7554/eLife.01322 Cannan, 2016, Mechanisms and consequences of double‐strand DNA break formation in chromatin, J. Cell. Physiol., 231, 3, 10.1002/jcp.25048 Caplin, 2018, Ionizing radiation, higher plants, and radioprotection: from acute high doses to chronic low doses, Front. Plant Sci., 9, 10.3389/fpls.2018.00847 Culligan, 2006, ATR and ATM play both distinct and additive roles in response to ionizing radiation, Plant J., 48, 947, 10.1111/j.1365-313X.2006.02931.x De Micco, 2011, Effects of sparsely and densely ionizing radiation on plants, Radiat. Environ. Biophys., 50, 1, 10.1007/s00411-010-0343-8 De Schutter, 2007, Arabidopsis WEE1 kinase controls cell cycle arrest in response to activation of the DNA integrity checkpoint, Plant Cell, 19, 211, 10.1105/tpc.106.045047 Della Rovere, 2016, The quiescent center and the stem cell niche in the adventitious roots of Arabidopsis thaliana, Plant Signal. Behav., 11, 10.1080/15592324.2016.1176660 Dewil, 2017, New perspectives for advanced oxidation processes, J. Environ. Manag., 195, 93, 10.1016/j.jenvman.2017.04.010 Dighton, 2008, Fungi and ionizing radiation from radionuclides, FEMS Microbiol. Lett., 281, 109, 10.1111/j.1574-6968.2008.01076.x Doucet-Chabeaud, 2001, Ionising radiation induces the expression of PARP-1 and PARP-2 genes in Arabidopsis, Mol. Genet. Genom., 265, 954, 10.1007/s004380100506 Doutriaux, 1998, Isolation and characterisation of the RAD51 and DMC1 homologs from Arabidopsis thaliana, Mol. Gen. Genet., 257, 283, 10.1007/s004380050649 Dutta, 2018, Oxidative and genotoxic damages in plants in response to heavy metal stress and maintenance of genome stability, Plant Signal. Behav., 13 Esnault, 2010, Ionizing radiation: advances in plant response, Environ. Exp. Bot., 68, 231, 10.1016/j.envexpbot.2010.01.007 Exposito-Alonso, 2018, The rate and potential relevance of new mutations in a colonizing plant lineage, PLoS Genet., 14, 10.1371/journal.pgen.1007155 Feng, 2013, A conversation across generations: soma-germ cell crosstalk in plants, Dev. Cell, 24, 215, 10.1016/j.devcel.2013.01.014 Fesenko, 2019, Review of radiation effects in non-human species in areas affected by the Kyshtym accident, J. Radiol. Prot., 39, R1, 10.1088/1361-6498/aafa92 Foray, 2016, Individual response to ionizing radiation, Mutat. Res., 770, 369, 10.1016/j.mrrev.2016.09.001 Fujimori, 2014, Plant DNA-damage repair/toleration 100 protein repairs UV-B-induced DNA damage, DNA Repair, 21, 171, 10.1016/j.dnarep.2014.05.009 Furlong, 2012, Expression of genes involved in a radiation-induced bystander effect, Mutagenesis, 27, 125 Garnier-Laplace, 2013, Are radiosensitivity data derived from natural field conditions consistent with data from controlled exposures? A case study of Chernobyl wildlife chronically exposed to low dose rates, J. Environ. Radioact., 121, 12, 10.1016/j.jenvrad.2012.01.013 Geras'Kin, 2008, Effects of non-human species irradiation after the Chernobyl NPP accident, Environ. Int., 34, 880, 10.1016/j.envint.2007.12.012 Gill, 2015 Hefner, 2006, Tissue-specific regulation of cell-cycle responses to DNA damage in Arabidopsis seedlings, DNA Repair, 5, 102, 10.1016/j.dnarep.2005.08.013 Hinton, 2007, Radiation-induced effects on plants and animals: findings of the united nations Chernobyl forum, Health Phys., 93, 427, 10.1097/01.HP.0000281179.03443.2e Hong, 2018, Comparison of radiosensitivity response to acute and chronic gamma irradiation in colored wheat, Genet. Mol. Biol., 41, 611, 10.1590/1678-4685-gmb-2017-0189 Horemans, 2018, Genome-wide DNA methylation changes in two Brassicaceae species sampled alongside a radiation gradient in Chernobyl and Fukushima, J. Environ. Radioact., 192, 405, 10.1016/j.jenvrad.2018.07.012 Hu, 2016, H2O2 and Ca2+-based signaling and associated ion accumulation, antioxidant systems and secondary metabolism orchestrate the response to NaCl stress in perennial ryegrass, Sci. Rep., 6, 10.1038/srep36396 I Azzam, 2012, Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury, Canc. Lett., 327, 48, 10.1016/j.canlet.2011.12.012 Jin, 2011, DNA methylation: superior or subordinate in the epigenetic hierarchy?, Genes Canc., 2, 607, 10.1177/1947601910393957 Kal'Chenko, 2001, Genetic effects of acute and chronic ionizing irradiation on Pinus sylvestris L. Inhabiting the Chernobyl meltdown area, Genetika, 37, 437 Khan, 2020, Melatonin: awakening the defense mechanisms during plant oxidative stress, Plants, 9, 10.3390/plants9040407 Kim, 2007, Transcriptomic profile of Arabidopsis rosette leaves during the reproductive stage after exposure to ionizing radiation, Radiat. Res., 168, 267, 10.1667/RR0963.1 Koike, 2001, Leaf morphology and photosynthetic adjustments among deciduous broad-leaved trees within the vertical canopy profile, Tree Physiol., 21, 951, 10.1093/treephys/21.12-13.951 Kovalchuk, 2000, Wheat mutation rate after Chernobyl, Nature, 407, 583, 10.1038/35036692 Kovalchuk, 2003, Genome hypermethylation in Pinus silvestris of Chernobyl-a mechanism for radiation adaptation?, Mutat. Res., 529, 13, 10.1016/S0027-5107(03)00103-9 Kovalchuk, 2004, Molecular aspects of plant adaptation to life in the Chernobyl zone, Plant Physiol., 135, 357, 10.1104/pp.104.040477 Kovalchuk, 2007, Transcriptome analysis reveals fundamental differences in plant response to acute and chronic exposure to ionizing radiation, Mutat. Res., 624, 101, 10.1016/j.mrfmmm.2007.04.009 Kumar, 2018, Epigenetics of modified DNA bases: 5-methylcytosine and beyond, Front. Genet., 9, 10.3389/fgene.2018.00640 Lanfear, 2018, Do plants have a segregated germline?, PLoS Biol., 16, 10.1371/journal.pbio.2005439 Lennicke, 2015, Hydrogen peroxide–production, fate and role in redox signaling of tumor cells, Cell Commun. Signal., 13, 10.1186/s12964-015-0118-6 Lethin, 2020, Development and characterization of an EMS-mutagenized wheat population and identification of salt-tolerant wheat lines, BMC Plant Biol., 20, 10.1186/s12870-019-2137-8 Lieber, 2010, The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway, Annu. Rev. Biochem., 79, 181, 10.1146/annurev.biochem.052308.093131 Lomax, 2013, Biological consequences of radiation-induced DNA damage: relevance to radiotherapy, Clin. Oncol., 25, 578, 10.1016/j.clon.2013.06.007 Ma, 2010, Development of flowering plant gametophytes, Curr. Top. Dev. Biol., 91, 379, 10.1016/S0070-2153(10)91013-2 Manova, 2015, DNA damage and repair in plants – from models to crops, Front. Plant Sci., 6, 10.3389/fpls.2015.00885 Maynard, 2009, Base excision repair of oxidative DNA damage and association with cancer and aging, Carcinogenesis, 30, 2, 10.1093/carcin/bgn250 Merrifield, 2013, Epigenetics in radiation biology: a new research frontier, Front. Genet., 4, 10.3389/fgene.2013.00040 Moura, 2010, Abiotic and biotic stresses and changes in the lignin content and composition in plants, J. Integr. Plant Biol., 52, 360, 10.1111/j.1744-7909.2010.00892.x Mousseau, 2014, Genetic and ecological studies of animals in Chernobyl and Fukushima, J. Hered., 105, 704, 10.1093/jhered/esu040 Nisa, 2019, The plant DNA damage response: signaling pathways leading to growth inhibition and putative role in response to stress conditions, Front. Plant Sci., 10, 10.3389/fpls.2019.00653 2003 O'Dea, 2016, The role of non-genetic inheritance in evolutionary rescue: epigenetic buffering, heritable bet hedging and epigenetic traps, Environ. Epigenet., 2 Panchy, 2016, Evolution of gene duplication in plants, Plant Physiol., 171, 2294, 10.1104/pp.16.00523 Pierrugues, 2001, Lipid phosphate phosphatases in Arabidopsis. Regulation of the AtLPP1 gene in response to stress, J. Biol. Chem., 276, 20300, 10.1074/jbc.M009726200 Preuss, 2003, A DNA-damage-induced cell cycle checkpoint in Arabidopsis, Genetics, 164, 323, 10.1093/genetics/164.1.323 Puglielli, 2017, Short-term physiological plasticity: trade-off between drought and recovery responses in three Mediterranean Cistus species, Ecol Evol, 7, 10880, 10.1002/ece3.3484 Ravanat, 2016, UV and ionizing radiations induced DNA damage, differences and similarities, Radiat. Phys. Chem., 128, 92, 10.1016/j.radphyschem.2016.07.007 Real, 2004, Effects of ionising radiation exposure on plants, fish and mammals: relevant data for environmental radiation protection, J. Radiol. Prot., 24, A123, 10.1088/0952-4746/24/4A/008 Reisz, 2014, Effects of ionizing radiation on biological molecules—mechanisms of damage and emerging methods of detection, Antioxidants Redox Signal., 21, 260, 10.1089/ars.2013.5489 Rodgers, 2008, Radio-adaptive response to environmental exposures at Chernobyl, Dose-Response, 6, 209, 10.2203/dose-response.07-008.Rodgers Rodgers, 2016, Error-prone repair of DNA double-strand breaks, J. Cell. Physiol., 231, 15, 10.1002/jcp.25053 Sacks, 2016, Epidemiology without biology: false paradigms, unfounded assumptions, and specious statistics in radiation science (with commentaries by Inge Schmitz-Feuerhake and Christopher Busby and a reply by the authors), Biol. Theory, 11, 69, 10.1007/s13752-016-0244-4 Song, 2015, PARP2 is the predominant poly (ADP-ribose) polymerase in Arabidopsis DNA damage and immune responses, PLoS Genet., 11, 10.1371/journal.pgen.1005200 Steinhauser, 2014, Comparison of the Chernobyl and Fukushima nuclear accidents: a review of the environmental impacts, Sci. Total Environ., 470 Trapp, 2011, Homologs of breast cancer genes in plants, Front. Plant Sci., 2, 10.3389/fpls.2011.00019 Vandenhove, 2010, Life-cycle chronic gamma exposure of Arabidopsis thaliana induces growth effects but no discernible effects on oxidative stress pathways, Plant Physiol. Biochem., 48, 778, 10.1016/j.plaphy.2010.06.006 Vives i Batlle, 2015, Exposures and effects in the marine environment after the Fukushima accident, Ann. ICRP, 44, 331, 10.1177/0146645315576099 Volkova, 2017, Radiation exposure in the remote period after the Chernobyl accident caused oxidative stress and genetic effects in Scots pine populations, Sci. Rep., 7, 10.1038/srep43009 Walker, 2004, Plant succession as an integrator of contrasting ecological time scales, Trends Ecol. Evol., 29, 504, 10.1016/j.tree.2014.07.002 Wang, 2016, Ultraviolet-B-induced DNA damage and ultraviolet-B tolerance mechanisms in species with different functional groups coexisting in subalpine moorlands, Oecologia, 181, 1069, 10.1007/s00442-016-3644-z Watson, 2016, Germline replications and somatic mutation accumulation are independent of vegetative life span in Arabidopsis, Proc. Natl. Acad. Sci. U.S.A., 113, 12226, 10.1073/pnas.1609686113 Weiss, 2011, Distribution pattern of artificial radionuclides in the Baltic Sea in the special event of the Chernobyl fallout, Isotopes, Environ. Health. Stud., 47, 254, 10.1080/10256016.2011.602475 West, 2000, Arabidopsis DNA ligase IV is induced by γ‐irradiation and interacts with an Arabidopsis homologue of the double strand break repair protein XRCC4, Plant J., 24, 67, 10.1046/j.1365-313x.2000.00856.x Whicker, 1997, Health impacts of large releases of radionuclides. Impacts on plant and animal populations, Ciba Found. Symp., 203, 74 Woodwell, 1967, Effects of chronic gamma irradiation on lichen communities of a forest, Am. J. Bot., 54, 1210, 10.1002/j.1537-2197.1967.tb10756.x Woodwell, 1963, Chronic gamma radiation affects the distribution of radial increment in Pinus rigida stems, Science, 139, 222, 10.1126/science.139.3551.222 Wright, 2018, Homologous recombination and the repair of DNA double-strand breaks, J. Biol. Chem., 293, 10524, 10.1074/jbc.TM118.000372 Wu, 2014, Reversing DNA methylation: mechanisms, genomics, and biological functions, Cell, 156, 45, 10.1016/j.cell.2013.12.019 Yu, 2016, 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., 12, 10.1371/journal.pgen.1006175 Zaichkina, 2004, Low doses of gamma-radiation induce nonlinear dose responses in mammalian and plant cells, Nonlinearity Biol. Toxicol. Med., 2, 213, 10.1080/15401420490519861 Zaka, 2002, Effects of low chronic doses of ionizing radiation on antioxidant enzymes and G6PDH activities in Stipa capillata (Poaceae), J. Exp. Bot., 53, 1979, 10.1093/jxb/erf041