, Volume 250, Issue 5, pp 1567–1590 | Cite as

Comparative sensitivity to gamma radiation at the organismal, cell and DNA level in young plants of Norway spruce, Scots pine and Arabidopsis thaliana

  • Dajana Blagojevic
  • YeonKyeong Lee
  • Dag A. Brede
  • Ole Christian Lind
  • Igor Yakovlev
  • Knut Asbjørn Solhaug
  • Carl Gunnar Fossdal
  • Brit Salbu
  • Jorunn E. OlsenEmail author
Original Article


Main conclusion

Persistent DNA damage in gamma-exposed Norway spruce, Scots pine and Arabidopsis thaliana, but persistent adverse effects at the organismal and cellular level in the conifers only.

Gamma radiation emitted from natural and anthropogenic sources may have strong negative impact on plants, especially at high dose rates. Although previous studies implied different sensitivity among species, information from comparative studies under standardized conditions is scarce. In this study, sensitivity to gamma radiation was compared in young seedlings of the conifers Scots pine and Norway spruce and the herbaceous Arabidopsis thaliana by exposure to 60Co gamma dose rates of 1–540 mGy h−1 for 144 h, as well as 360 h for A. thaliana. Consistent with slightly less prominent shoot apical meristem, in the conifers growth was significantly inhibited with increasing dose rate ≥ 40 mGy h−1. Post-irradiation, the conifers showed dose-rate-dependent inhibition of needle and root development consistent with increasingly disorganized apical meristems with increasing dose rate, visible damage and mortality after exposure to ≥ 40 mGy h−1. Regardless of gamma duration, A. thaliana showed no visible or histological damage or mortality, only delayed lateral root development after ≥ 100 mGy h−1 and slightly, but transiently delayed post-irradiation reproductive development after ≥ 400 mGy h−1. In all species dose-rate-dependent DNA damage occurred following ≥ 1–10 mGy h−1 and was still at a similar level at day 44 post-irradiation. In conclusion, the persistent DNA damage (possible genomic instability) following gamma exposure in all species may suggest that DNA repair is not necessarily mobilized more extensively in A. thaliana than in Norway spruce and Scots pine, and the far higher sensitivity at the organismal and cellular level in the conifers indicates lower tolerance to DNA damage than in A. thaliana.


DNA damage Development Growth Ionizing radiation Picea abies Pinus sylvestris 



The Norwegian Research Council through its Centre of Excellence funding scheme (Grant 223268/F50) and the Norwegian University of Life Sciences (among others PhD scholarship to DB) are acknowledged for financial support. Sincere thanks to Marit Siira and Ida K. Hagen for technical assistance in plant growing and Tone I. Melby and Dr. Marcos Viejo for advices in RT-qPCR analyses. Dr. Elisabeth L. Hansen is acknowledged for assistance in dosimetry work, and Dr. Gunnar Brunborg and staff members at the Norwegian Institute of Public Health for providing expertise and scoring facility for the COMET assay.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

Supplementary material

425_2019_3250_MOESM1_ESM.tif (2 mb)
Fig. S1 Phenotype of seedlings of (a) Norway spruce and (b) Scots pine plants at day 44 post-irradiation (day 56 after sowing) following exposure to gamma radiation at different dose rates (mGy h−1) for 144 h 7-12 days after sowing. (TIFF 2035 kb)
425_2019_3250_MOESM2_ESM.docx (13 kb)
Table S1 Oligonucleotide primer sequences used for RT-qPCR analyses of specific reference genes, DNA-repair-, antioxidant-, cell cycle- and defence-related-related genes in A. thaliana seedlings. (DOCX 12 kb)
425_2019_3250_MOESM3_ESM.docx (13 kb)
Table S2 Oligonucleotide primer sequences used for RT-qPCR analyses of specific reference genes, DNA-repair-, antioxidant-, cell cycle- and defence-related-related genes in Norway spruce seedlings. (DOCX 12 kb)
425_2019_3250_MOESM4_ESM.docx (13 kb)
Table S3 Oligonucleotide primer sequences used for RT-qPCR analyses of specific reference genes, DNA-repair-, antioxidant-, cell cycle- and defence-related-related genes in Scots pine seedlings. (DOCX 12 kb)


  1. Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30(3):161–175. CrossRefPubMedGoogle Scholar
  2. Amiro BD, Sheppard SC (1994) Effects of ionizing radiation on the boreal forest: Canada’s FIG experiment, with implications for radionuclides. Sci Total Environ 157:371–382. CrossRefGoogle Scholar
  3. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55(1):373–399. CrossRefPubMedGoogle Scholar
  4. Arkhipov NP, Kuchma ND, Askbrant S, Pasternak PS, Musica VV (1994) Acute and long-term effects of irradiation on pine (Pinus sylvestris) stands post-Chernobyl. Sci Total Environ 157:383–386. CrossRefPubMedGoogle Scholar
  5. Averbeck D, Salomaa S, Bouffler S, Ottolenghi A, Smyth V, Sabatier L (2018) Progress in low dose health risk research: novel effects and new concepts in low dose radiobiology. Mutat Res 776:46–69. CrossRefPubMedGoogle Scholar
  6. Aypar U, Morgan WF, Baulch JE (2011) Radiation-induced genomic instability: are epigenetic mechanisms the missing link? Int J Radiat Biol 87(2):179–191. CrossRefPubMedGoogle Scholar
  7. Azzam EI, Jay-Gerin JP, Pain D (2012) Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury. Cancer Lett 327:48–60. CrossRefPubMedGoogle Scholar
  8. Barescut J, Lariviere D, Stocki T, Vanhoudt N, Cuypers A, Vangronsveld J, Horemans N, Wannijn J, Van Hees M, Vandenhove H (2012) Study of biological effects and oxidative stress related responses in gamma irradiated Arabidopsis thaliana plants. Radioprotection 46(6):S401–S407. CrossRefGoogle Scholar
  9. Bassing CH, Chua KF, Sekiguchi J, Suh H, Whitlow SR, Fleming JC, Monroe BC, Ciccone DN, Yan C, Vlasakova K, Livingston DM, Ferguson DO, Scully R, Alt FW (2002) Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc Natl Acad Sci USA 99(12):8173–8178. CrossRefPubMedGoogle Scholar
  10. Belli M, Sapora O, Tabocchini MA (2002) Molecular targets in cellular response to ionizing radiation and implications in space radiation protection. J Radiat Res 43(Suppl):S13–S19CrossRefGoogle Scholar
  11. Caplin N, Willey N (2018) Ionizing radiation, higher plants, and radioprotection: from acute high doses to chronic low doses. Front Plant Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Culligan KM, Robertson CE, Foreman J, Doerner P, Britt AB (2006) ATR and ATM play both distinct and additive roles in response to ionizing radiation. Plant J 48(6):947–961. CrossRefPubMedGoogle Scholar
  13. De Micco V, Arena C, Pignalosa D, Durante M (2011) Effects of sparsely and densely ionizing radiation on plants. Radiat Environ Biophys 50(1):1–19. CrossRefPubMedGoogle Scholar
  14. De Veylder L, Larkin JC, Schnittger A (2011) Molecular control and function of endoreplication in development and physiology. Trends Plant Sci 16(11):624–634. CrossRefPubMedGoogle Scholar
  15. Deckbar D, Jeggo PA, Lobrich M (2011) Understanding the limitations of radiation-induced cell cycle checkpoints. Crit Rev Biotechnol 46(4):271–283. CrossRefGoogle Scholar
  16. Deflorio G, Horgan G, Woodward S, Fossdal CG (2011) Gene expression profiles, phenolics and lignin of Sitka spruce bark and sapwood before and after wounding and inoculation with Heterobasidion annosum. Physiol Mol Plant Pathol 75(4):180–187. CrossRefGoogle Scholar
  17. Donini B (1967) Effects of chronic gamma-irradiation on Pinus pinea and Pinus halepensis. Radiat Bot 7(3):183–192. CrossRefGoogle Scholar
  18. Esnault M-A, Legue F, Chenal C (2010) Ionizing radiation: advances in plant response. Environ Exp Bot 68(3):231–237. CrossRefGoogle Scholar
  19. Fesenko SV, Alexakhin RM, Geras’kin SA, Sanzharova NI, Spirin YV, Spiridonov SI, Gontarenko IA, Strand P (2005) Comparative radiation impact on biota and man in the area affected by the accident at the Chernobyl nuclear power plant. J Environ Radioact 80(1):1–25. CrossRefPubMedGoogle Scholar
  20. Fossdal CG, Yaqoob N, Krokene P, Kvaalen H, Solheim H, Yakovlev IA (2012) Local and systemic changes in expression of resistance genes, nb-lrr genes and their putative microRNAs in Norway spruce after wounding and inoculation with the pathogen Ceratocystis polonica. BMC Plant Biol 12:105. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gichner T, Patková Z, Kim JK (2003) DNA damage measured by the comet assay in eight agronomic plants. Biol Plant 47(2):185–188. CrossRefGoogle Scholar
  22. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930. CrossRefPubMedGoogle Scholar
  23. Goltsova N, Abaturov Y, Abaturov A, Melankholin P, Girbasova A, Rostova N (1991) Chernobyl radionuclide accident: effects on the shoot structure of Pinus sylvestris. Annales Botanici Fennici 28(1):1–13Google Scholar
  24. Hansen EL, Lind OC, Oughton DH, Salbu B (2019) A framework for exposure characterization and gamma dosimetry at the NMBU FIGARO irradiation facility. Int J Radiat Biol 95(1):82–89. CrossRefPubMedGoogle Scholar
  25. Hurem S, Gomes T, Brede DA, Lindbo Hansen E, Mutoloki S, Fernandez C, Mothersill C, Salbu B, Kassaye YA, Olsen A-K, Oughton D, Aleström P, Lyche JL (2017) Parental gamma irradiation induces reprotoxic effects accompanied by genomic instability in zebrafish (Danio rerio) embryos. Environ Res 159:564–578. CrossRefPubMedGoogle Scholar
  26. Kalisz S, Kramer EM (2007) Variation and constraint in plant evolution and development. Heredity 100:171. CrossRefPubMedGoogle Scholar
  27. Kashparova E, Levchuk S, Morozova V, Kashparov V (2018) A dose rate causes no fluctuating asymmetry indexes changes in silver birch (Betula pendula (L.) Roth.) leaves and Scots pine (Pinus sylvestris L.) needles in the Chernobyl Exclusion Zone. J Environ Radioact. CrossRefPubMedGoogle Scholar
  28. Kawai T, Inoshita T (1965) Effects of gamma ray irradiation on growing rice plants—I: irradiations at four main developmental stages. Radiat Bot 5(3):233–255. CrossRefGoogle Scholar
  29. Killion DD, Constantin MJ (1972) Gamma irradiation of corn plants: effects of exposure, exposure rate, and developmental stage on survival, height, and grain yield of two cultivars. Radiat Bot 12(3):159–164. CrossRefGoogle Scholar
  30. Kim JH, Chung BY, Kim JS, Wi SG (2005) Effects of in Planta gamma-irradiation on growth, photosynthesis, and antioxidative capacity of red pepper (Capsicum annuum L.) plants. J Plant Biol 48(1):47–56. CrossRefGoogle Scholar
  31. Kim DS, Kim JB, Goh EJ, Kim WJ, Kim SH, Seo YW, Jang CS, Kang SY (2011) Antioxidant response of Arabidopsis plants to gamma irradiation: genome-wide expression profiling of the ROS scavenging and signal transduction pathways. J Plant Physiol 168(16):1960–1971. CrossRefPubMedGoogle Scholar
  32. Koppen G, Azqueta A, Pourrut B, Brunborg G, Collins AR, Langie SAS (2017) The next three decades of the comet assay: a report of the 11th International Comet Assay Workshop. Mutagenesis 32(3):397–408CrossRefGoogle Scholar
  33. Kovalchuk O, Kovalchuk I, Titov V, Arkhipov A, Hohn B (1999) Radiation hazard caused by the Chernobyl accident in inhabited areas of Ukraine can be monitored by transgenic plants. Mutat Res Genetic Toxicol Environ Mutagen 446(1):49–55. CrossRefGoogle Scholar
  34. Kovalchuk I, Molinier J, Yao Y, Arkhipov A, Kovalchuk O (2007) Transcriptome analysis reveals fundamental differences in plant response to acute and chronic exposure to ionizing radiation. Mutat Res Fund Mol Mech Mutagen 624(1–2):101–113. CrossRefGoogle Scholar
  35. Kryshev II, Romanov GN, Isaeva LN, Kholina YB (1997) Radioecological state of lakes in the southern Ural impacted by radioactivity release of the 1957 radiation accident. J Environ Radioact 34(3):223–235. CrossRefGoogle Scholar
  36. Lee Y, Karunakaran C, Lahlali R, Liu X, Tanino KK, Olsen JE (2017) Photoperiodic Regulation of Growth-Dormancy Cycling through Induction of Multiple Bud-Shoot Barriers Preventing Water Transport into the Winter Buds of Norway Spruce. Front Plant Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Lind OC, Helen Oughton D, Salbu B (2018) The NMBU FIGARO low dose irradiation facility. Int J Radiat Biol. CrossRefPubMedGoogle Scholar
  38. Macovei A, Tuteja N (2013) Different expression of miRNAs targeting helicases in rice in response to low and high dose rate γ-ray treatments. Plant Signal Behav 8(8):e25128. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Makarenko ES, Oudalova AA, Geraskin SA (2016) Study of needle morphometric indices in Scots pine in the remote period after the Chernobyl accident. Radioprotection 51(1):19–23CrossRefGoogle Scholar
  40. Marcu D, Damian G, Cosma C, Cristea V (2013) Gamma radiation effects on seed germination, growth and pigment content, and ESR study of induced free radicals in maize (Zea mays). J Biol Phys 39(4):625–634. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51(345):659–668. CrossRefPubMedGoogle Scholar
  42. Mergen F, Strøm Johansen T (1964) Effect of ionizing radiation on seed germination and seedling growth of Pinus rigida (mill). Radiat Bot 4(4):417–427. CrossRefGoogle Scholar
  43. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9(10):490–498. CrossRefPubMedGoogle Scholar
  44. Morgan WF, Day JP, Kaplan MI, McGhee EM, Limoli CL (1996) Genomic instability induced by ionizing radiation. Radiat Res 146(3):247–258. CrossRefPubMedGoogle Scholar
  45. Mothersill C, Seymour CB (1998) Mechanisms and implications of genomic instability and other delayed effects of ionizing radiation exposure. Mutagenesis 13(5):421–426. CrossRefPubMedGoogle Scholar
  46. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3):473–497. CrossRefGoogle Scholar
  47. Nagata T, Todoriki S, Hayashi T, Shibata Y, Mori M, Kanegae H, Kikuchi S (1999) γ-Radiation induces leaf trichome formation in Arabidopsis. Plant Physiol 120(1):113–120CrossRefGoogle Scholar
  48. Olsen JE (2010) Light and temperature sensing and signaling in induction of bud dormancy in woody plants. Plant Mol Biol 73(1):37–47. CrossRefPubMedGoogle Scholar
  49. Paschoa AS (1998) Potential environmental and regulatory implications of naturally occurring radioactive materials (NORM). Appl Radiat Isot 49(3):189–196. CrossRefPubMedGoogle Scholar
  50. Reisz JA, Bansal N, Qian J, Zhao W, Furdui CM (2014) Effects of ionizing radiation on biological molecules—mechanisms of damage and emerging methods of detection. Antioxid Redox Signal 21(2):260–292. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Roldán-Arjona T, Ariza RR (2009) Repair and tolerance of oxidative DNA damage in plants. Mutat Res 681(2):169–179. CrossRefPubMedGoogle Scholar
  52. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386PubMedGoogle Scholar
  53. Rudolph TD (1971) Gymnosperm seedling sensitivity to gamma radiation: its relation to seed radiosensitivity and nuclear variables. Radiat Bot 11(1):45–51. CrossRefGoogle Scholar
  54. Sahr T, Voigt G, Schimmack W, Paretzke HG, Ernst D (2005) Low-level radiocaesium exposure alters gene expression in roots of Arabidopsis. New Phytol 168(1):141–148. CrossRefPubMedGoogle Scholar
  55. Sidorov VP (1994) Cytogenetic effect in Pinus sylvestris needle cells as a result of the Chernobyl accident. Radiat Biol 34(6):847–851Google Scholar
  56. Stalter R, Kincaid D (2009) Community development following gamma radiation at a pine–oak forest, Brookhaven National Laboratory, Long Island, New York1. Am J Bot 96(12):2206–2213. CrossRefPubMedGoogle Scholar
  57. Tikhomirov FA, Shcheglov AI (1994) Main investigation results on the forest radioecology in the Kyshtym and Chernobyl accident zones. Sci Total Environ 157:45–57. CrossRefPubMedGoogle Scholar
  58. Tulik M (2001) Cambial history of Scots pine trees (Pinus sylvestris) prior and after the Chernobyl accident as encoded in the xylem. Environ Exp Bot 46(1):1–10. CrossRefPubMedGoogle Scholar
  59. UNSCEAR (1996) Sources and effects of ionizing radiation. United Nations Scientific Commitee on the Effects of Atomic Radiation, New YorkGoogle Scholar
  60. UNSCEAR (2017) Sources, effects and risks of ionizing radiation. United Nations Scientific Commitee on the Effects of Atomic Radiation, New YorkGoogle Scholar
  61. van de Walle J, Horemans N, Saenen E, Van Hees M, Wannijn J, Nauts R, van Gompel A, Vangronsveld J, Vandenhove H, Cuypers A (2016) Arabidopsis plants exposed to gamma radiation in two successive generations show a different oxidative stress response. J Environ Radioact 165:270–279. CrossRefPubMedGoogle Scholar
  62. Van Hoeck A, Horemans N, Van Hees M, Nauts R, Knapen D, Vandenhove H, Blust R (2015) Characterizing dose response relationships: chronic gamma radiation in Lemna minor induces oxidative stress and altered polyploidy level. J Environ Radioact 150:195–202. CrossRefPubMedGoogle Scholar
  63. Van Hoeck A, Horemans N, Nauts R, Van Hees M, Vandenhove H, Blust R (2017) Lemna minor plants chronically exposed to ionising radiation: RNA-seq analysis indicates a dose rate dependent shift from acclimation to survival strategies. Plant Sci 257:84–95. CrossRefPubMedGoogle Scholar
  64. Vandenhove H, Vanhoudt N, Cuypers A, van Hees M, Wannijn J, Horemans N (2010) Life-cycle chronic gamma exposure of Arabidopsis thaliana induces growth effects but no discernable effects on oxidative stress pathways. Plant Physiol Biochem 48(9):778–786. CrossRefPubMedGoogle Scholar
  65. Vives i Batlle J, Aono T, Brown JE, Hosseini A, Garnier-Laplace J, Sazykina T, Steenhuisen F, Strand P (2014) The impact of the Fukushima nuclear accident on marine biota: retrospective assessment of the first year and perspectives. Sci Total Environ 487:143–153. CrossRefPubMedGoogle Scholar
  66. Watanabe Y, Se Ichikawa, Kubota M, Hoshino J, Kubota Y, Maruyama K, Fuma S, Kawaguchi I, Yoschenko VI, Yoshida S (2015) Morphological defects in native Japanese fir trees around the Fukushima Daiichi Nuclear Power Plant. Sci Rep 5:13232. CrossRefPubMedPubMedCentralGoogle Scholar
  67. Wi SG, Chung BY, Kim JH, Baek MH, Yang DH, Lee JW, Kim JS (2005) Ultrastructural changes of cell organelles in Arabidopsis stems after gamma irradation. J Plant Biol 48(2):195–200. CrossRefGoogle Scholar
  68. Wi SG, Chung BY, Kim J-S, Kim J-H, Baek M-H, Lee J-W, Kim YS (2007) Effects of gamma irradiation on morphological changes and biological responses in plants. Micron 38(6):553–564. CrossRefPubMedGoogle Scholar
  69. Woodwell GM (1962) Effects of ionizing radiation on terrestrial ecosystems. Experiments show how ionizing radiation may alter normally stable patterns of ecosystem behavior. Science 138(3540):572–577. CrossRefPubMedGoogle Scholar
  70. Woodwell GM, Rebuck AL (1967) Effects of chronic gamma radiation on the structure and diversity of an oak-pine forest. Ecol Monogr 37(1):53–69. CrossRefGoogle Scholar
  71. Wright SI, Gaut BS (2005) Molecular population genetics and the search for adaptive evolution in plants. Mol Biol Evol 22(3):506–519. CrossRefPubMedGoogle Scholar
  72. Yoschenko V, Ohkubo T, Kashparov V (2017) Radioactive contaminated forests in Fukushima and Chernobyl. J For Res. CrossRefGoogle Scholar
  73. Yoshiyama K, Conklin PA, Huefner ND, Britt AB (2009) Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage. Proc Natl Acad Sci USA 106(31):12843–12848. CrossRefPubMedGoogle Scholar
  74. Yoshiyama KO, Sakaguchi K, Kimura S (2013) DNA damage response in plants: conserved and variable response compared to animals. Biology 2(4):1338–1356. CrossRefPubMedPubMedCentralGoogle Scholar
  75. Zelena L, Sorochinsky B, von Arnold S, van Zyl L, Clapham DH (2005) Indications of limited altered gene expression in Pinus sylvestris trees from the Chernobyl region. J Environ Radioact 84(3):363–373. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Dajana Blagojevic
    • 1
    • 2
  • YeonKyeong Lee
    • 1
    • 2
  • Dag A. Brede
    • 2
    • 3
  • Ole Christian Lind
    • 2
    • 3
  • Igor Yakovlev
    • 4
  • Knut Asbjørn Solhaug
    • 2
    • 3
  • Carl Gunnar Fossdal
    • 4
  • Brit Salbu
    • 2
    • 3
  • Jorunn E. Olsen
    • 1
    • 2
    Email author
  1. 1.Department of Plant Sciences, Faculty of BiosciencesNorwegian University of Life SciencesÅsNorway
  2. 2.Centre of Environmental Radioactivity (CERAD), Norwegian University of Life SciencesÅsNorway
  3. 3.Faculty of Environmental Sciences and Natural Resource ManagementNorwegian University of Life SciencesÅsNorway
  4. 4.Norwegian Institute of Bioeconomy ResearchÅsNorway

Personalised recommendations