Effects of chronic radiation exposure on the plant populations, observed in the reference plant the Scots Pine. Reveiw

«Radiation and Risk», 2018, vol. 27, No. 4, pp.95-118

DOI: 10.21870/0131-3878-2018-27-4-95-118

Authors

Geras’kin S.A. – Head of Lab, D. Sc., Biol., Prof. Contacts: 109 km, Kievskoe Sh., Obninsk, Kaluga region, Russia, 249032. Tel. (484) 399-69-64; e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it. .
Volkova P.Yu. – Leading Researcher, C. Sc., Biol.
Kazakova E.A. – Researcher.
Vasiliyev D.V. – Senior Researcher, C. Sc., Biol.
Dikareva N.S. – Researcher, C. Sc., Agr.
Makarenko E.S. – Researcher.
Kuzmenkov A.G. – Junior Researcher
Oudalova A.A.¹ – D. Sc., Biol., Prof.
Duarte G.T.² – Postdoc Researcher. Institut Jean-Pierre Bourgin (IJPB).

Russian Institute of Radiology and Agroecology, Obninsk
¹Obninsk Institute for Nuclear Power Engineering, Obninsk
²Institute Jean-Pierre Bourgin, Versailles, France

Abstract

Large-scale radiation accidents at the Mayak production association and at the Chernobyl NPP caused contamination of large territories of Russia by radioactive fallouts. The increased level of mutagenesis found in plants and animals inhabiting radioactively contaminated lands raise the question about possible ecological consequences of chronic exposure to low-dose radiation. However, late effects of chronic exposure to radiation on plants and animals are still debated in scientific communities. The paper presents the basic results of long-term follow up (2003-2016) of the populations of the Scots pine inhabiting in areas with different levels and spectrum of radioactive contamination. Population of animals and plants developing under continuous radiation exposure have increased levels of mutagenesis, genome wide methylation, changes in genes expression, genetic structure of the population and temporal dynamics of cytogenetic defects. However, found genetic changes in the pine organism did not affect enzyme activity in endosperms, rates of morphologic abnormalities and rates of reproductive power. Results of the study provide evidence that the pine has high sensitivity to chronic radiation exposure. Significant genetic effects had been observed during the surveillance period, perhaps these effects will be observed for a long time. Since changes in epigenetic status and genetic structures of the edificator plant, the Scots pine is one of the environment-forming plants playing important role in forming response of the environment to radiation, these processes should be taken into account when programs on the preservation of biodiversity under chronic radiation exposure are developed.

Key words
Accident at the Chernobyl NPP, Scots pine, chronic exposure to radiation, absorbed doses, mutations in isoenzyme loci, cytogenetic effects, population genetic structure, genome methylation, expression of genes, morphologic abnormalities, reproductive power.ronmental factors, woodsmoke, wildfires, prenatal, postnatal, children, carcinogenesis, leukemia, system analysis.

References

1. Geras’kin S.A. Ecological effects of exposure to enhanced levels of ionizing radiation. J. Environ. Radioact., 2016, vol. 162-163, pp. 347-357.

2. Ellison A.M., Bank M.S., Clinton B.D., Colburn E.A., Elliott K., Ford C.R., Foster D.R., Kloeppel B.D., Knoepp J.D., Lovett G.M., Mohan J., Orwig D.A., Rodenhouse N.L., Sobczak W.V., Stinson K.A., Stone J.K., Swan C.M., Thompson J., Holle B.V., Webster J.R. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front. Ecol. Environ., 2005, vol. 3, pp. 479-486.

3. Atlas of modern and predictive aspects of the Chernobyl NPP accident in the affected areas of Russia and Belarus. Mocsow-Minsk, Belcartographia, 2009. 140 p. (In Russian).

4. Geras’kin S.A., Evseeva T.I., Oudalova A.A. Plants as a tool for the environmental health assessment. Encyclopedia of Environmental Health. Burlington, Elsevier, 2011, vol. 4, pp. 571-579.

5. Glazko T.T., Arkhipov N.P., Glazko V.I. Population-genetic consequences of environmental accidents on the example of the Chernobyl accident. Moscow, Moscow Agricultural Academy, 2008. 556 p. (In Russian).

6. Pozolotina V.N., Molchanova I.V., Karavaeva E.N., Mikhailovskaya L.N., Antonova E.V. Current state of the terrestrial ecosystems of the East Ural radioactive trace: levels of pollution and biological effects. Yekaterinburg, Goschitsy, 2008. 204 p. (In Russian).

7. Shevchenko V.A., Pechkurenkov V.L., Abramov V.I. Radiation genetics of natural populations: genetic consequences of the Kyshtym accident. Moscow, Nauka, 1992. 221 p. (In Russian).

8. Moller A.P., Mousseau T.A. Strong effects of ionizing radiation from Chernobyl on mutation rates. Sci. Reports, 2014, vol. 5, 8363.

9. Boubryak I., Akimkina T., Polischuk V., Dmitriev A., MacCready S., Grodzinsky D. Long-term effects of Chernobyl contamination on DNA repair function and plant resistance to different biotic and abiotic stress factors. Tsitologiya i genetika – Cytology and Genetics, 2016, vol. 50, no. 6, pp. 34-59.

10. Geras'kin S.A., Evseeva T.I., Oudalova A.A. Effects of long-term chronic exposure to radionuclides in plant populations. J. Environ. Radioact., 2013, vol. 121, pp. 22-32.

11. Omar-Nazir L., Shi X., Moller A., Mousseaau T., Byun S., Hancock S., Seymour C., Mothersill C. Long-term effects of ionizing radiation after the Chernobyl accident: possible contribution of historic dose. Environ. Res., 2018, vol. 165, pp. 55-62.

12. Fuller N., Smith J.T., Nagorskaya L.L., Gudkov D.I., Ford A.T. Does Chernobyl-derived radiation impact the developmental stability of Asellus aquaticus 30 years on? Sci. Tot. Environ., 2017, vol. 576, pp. 242-250.

13. Fuller N., Ford A.T., Nagorskaya L.L., Gudkov D.I., Smith J.T. Reproduction in the freshwater crustacean Asellus aquaticus along a gradient of radionuclide contamination at Chernobyl. Sci. Tot. Environ., 2018, vol. 628-629, pp. 11-17.

14. Deryabina T., Kuchmel S., Nagorskaya L., Hinton T., Beasley J., Lerebours A., Smith J. Long-term census data reveal abundant wildlife populations at Chernobyl. Cur. Biol., 2015, vol. 25, pp. R824-R826.

15. Møller A.P., Mousseau T.A. Assessing effects of radiation on abundance of mammals and predator-prey interactions in Chernobyl using tracks in the snow. Ecol. Indic., 2013, vol. 26, pp. 112-116.

16. Webster S.C., Byrne M.E., Lance S.L., Love C.N., Hinton T.G., Shamovich D., Beasley J.C. Where the wild things are: influence of radiation on the distribution of four mammalian species within the Chernobyl exclusion zone. Front. Ecol. Environ., 2016, vol. 14, pp. 185-190.

17. Lerebours A., Gudkov D., Nagorskaya L., Kaglyan A., Rizewski V., Leshchenko A., Bailey E.H., Bakir A., Ovsyanikova S., Laptev G., Smith J.T. Impact of environmental radiation on the health and reproductive status of fish from Chernobyl. Environ. Sci. Technol., 2018, vol. 52, pp. 9442-9450.

18. Caplin N., Willey N. Ionizing radiation, higher plants, and radioprotection: from acute high doses to chronic low doses. Front. Plant Sci., 2018, vol. 9, p. 847.

19. Grodzinsky D.M. Radiobiology of plants. Kiev: Naukova Dumka, 1989. 384 p. (In Russian).

20. ICRP Publication 108. Environmental protection: the concept and use of reference animals and plants. Ann. ICRP, 2009, vol. 38, pp. 1-242.

21. Kozubov G.M., Taskaev A.I. Radiobiological and radioecological studies of woody plants. S.-P., Nauka, 1994. 256 p. (In Russian).

22. Verta J-P., Landry C.R., Mackay J.J. Are long-lived trees poised for evolutionary change? Single locus effects in the evolution of gene expression networks in spruce. Mol. Ecol., 2013, vol. 22, pp. 2369-2379.

23. Geras’kin S., Oudalova A., Dikareva N., Spiridonov S., Hinton T., Chernonog E., Garnier-Laplace J. Effects of radioactive contamination on Scots pines in the remote period after the Chernobyl accident. Ecotoxicol., 2011, vol. 20, pp. 1195-1208.

24. Spiridonov S.I., Fesenko S.V., Geras’kin S.A., Solomatin V.M., Karpenko Ye.I. The dose estimation of woody plants in the remote period after the Chernobyl NPP accident. Radiatsionnaya biologiya. Radioekologiya – Radiation Biology. Radioecology, 2008, vol. 48, no. 4, pp. 432-438. (In Russian).

25. Geras’kin S.A., Dikareva N.S., Oudalova А.А., Vasil’ev D.V., Volkova P.Yu. The consequences of chronic radiation exposure of Scots pine in the remote period after the Chernobyl accident. Russian Journal of Ecology, 2016, vol. 47, pp. 26-38.

26. Makarenko E.S., Oudalova А.А., Geras’kin S.А. Morphometric indices of Scots pine needles under Chronic exposure of radiation. Contemporary Problems of Ecology, 2017, vol. 10, pp. 761-769.

27. Geras’kin S., Volkova P. Genetic diversity in Scots pine populations along a radiation exposure gradient. Sci. Tot. Environ., 2014, vol. 496, pp. 317-327 (In Russian).

28. Volkova P.Yu., Geras’kin S.A., Kazakova E.A. Radiation exposure in the remote period after the Chernobyl accident caused oxidative stress and genetic effects in Scots pine populations. Scientific Reports, 2017, vol. 7, p. 43009.

29. Volkova P.Yu., Geras’kin S.A., Horemans N., Makarenko E.S., Saenen E., Nauts R., Bondarenko V.S., Duarte G.T., Jacobs G., Voorspoels S., Kudin M. Chronic radiation exposure as an ecological factor: hypermethylation and genetic differentiation in irradiated Scots pine populations. Environ. Pollution, 2018, vol. 232, pp. 105-112.

30. Streffer C., Bolt H., Follesdal D., Hall P., Hengstler J.G., Jakob P., Oughton D., Prieb K., Rehbinder E., Swaton E. Low dose exposures in the environment. Dose-effect relations and risk evaluation. Berlin Heidelberg, Springer-Verlag, 2004. 471 p.

31. Geras’kin S.А., Kuzmenkov А.G., Vasiliyev D.V. Time dynamics of cytogenetic effects in chronically ex-posed Scots pine populations. Radiatsionnaya biologiya. Radioekologiya – Radiation Biology. Radioecology, 2018, vol. 58, no. 1, pp. 74-84. (In Russian).

32. Geras’kin S., Oudalova A., Kuzmenkov A., Vasiliyev D. Chronic radiation exposure modifies temporal dynamics of cytogenetic but not reproductive indicators in Scots pine populations. Environ. Pollution, 2018, vol. 239, pp. 399-407.

33. Oudalova А.А., Geras’kin S.А. The time dynamics and ecological-genetic variation of cytogenetic effects in the Scots pine populations experiencing anthropogenic impact. Biology Bulletin Reviews, 2012, vol. 2, no. 3, pp. 254-267.

34. Dubinin N.P., Tiniakov G.G. Inversion gradients and natural selection in ecological races of Drosophila funebris. Genetics, 1946, vol. 31, pp. 537-545.

35. Theodorakis C.W. Integration of genotoxic and population genetic endpoints in biomonitoring and risk as-sessment. Ecotoxicol., 2001, vol. 10, pp. 245-256.

36. Kazakova Е.А., Volkova P.Yu., Geras’kin S.А. Analysis of changes in the genetic structure of chronically irradiated Scots pine populations. Russian J. Genetics: Applied Research, 2018, vol. 8, no. 2, pp. 124-134.

37. Guries R.P., Ledig F.T. Genetic diversity and population structure in Pitch pine (Pinus rigida Mill.). Evolution, 1982, vol. 36, pp. 387-402.

38. Krutovsky K.V., Politov D.V., Altukhov Yu.P., Milutin L.I., Kuznetsova G.V., Proshnikov A.I., Vorobiov V.N., Vorobiova N.A. Genetic variability in Siberian cedar pine, Pinus Sibirica Du TOUR. IV. Genetic diversity and differentiation between populations. Genetika – Russian Journal of Genetics, 1989, vol. 25, no. 11, pp. 2009-2032. (In Russian).

39. Ulianova E.V., Pozolotina V.N., Sarapult’sev I.E. Ecological-genetic characteristics of coenopopulations of Taraxacum officinales L from the flood lands of the Techa River. Russian Journal of Ecology, 2004, vol. 35, pp. 349-357.

40. Sarapult’zev B.I., Geras’kin S.A. Genetic basis of radioresistance and evolution. Moscow, Energoatomizdat Publishers, 1993. 208 p. (In Russian).

41. Pozolotina V.N., Antonova E.V., Bezel V.S. Comparison of remote consequences in Taraxacum officinale seed progeny collected in radioactively or chemically contaminated areas. Ecotoxicol., 2012, vol. 21, pp. 1979-1988.

42. Banks S.C., Cary G.J., Smith A.L., Davies I.D., Driscoll D.A., Gill A.M., Lindenmayer D.B., Peakall R. How does ecological disturbance influence genetic diversity? Trends Ecol. Evol., 2013, vol. 28, pp. 670-679.

43. Kuchma O., Finkeldey R. Evidence for selection in response to radiation exposure: Pinus sylvestris in the Chernobyl exclusion zone. Environ. Pollution, 2011, vol. 159, pp. 1606-1612.

44. Altukhov Yu.P. Genetic processes in populations. Moscow, Akademkniga, 2003. 431 p. (In Russian).

45. Sahu P.P., Pandey G., Sharma N., Puranik S., Muthamilarasan M., Prasad M. Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep., 2013, vol. 32, pp. 1151-1159.

46. Kovalchuk O., Burke P., Arkhipov A., Kuchma N., James S.J., Kovalchuk I., Pogribny I. Genome hypermethylation in Pinus sylvestris of Chernobyl – a mechanism for radiation adaptation? Mutat. Res., 2003, vol. 529, pp. 13-20.

47. Rabinowicz P.D., Palmer L.E., May B.P., Hemann M.T., Lowe S.W., McCombie W.R., Martienssen R.A. Genes and transposons are differentially methylated in plants, but not in mammals. Genome Res., 2003, vol. 13, pp. 2658-2664.

48. Ikeda Y., Nishimura T. Nuclear functions in plant transcription, signaling and development. Chapter 2. The role of DNA methylation in transposable element silencing and genomic imprinting. New York, Springer Science+Business Media, 2015. P. 13-29.

49. Duarte G.T., Volkova P.Yu., Geras’kin S.A. Delineating the functional pattern of adaptation to chronic radiation exposure by the transcriptome analysis of Scots pine from the Chernobyl exclusion zone. Nat. Ecol. Evol., under review.

50. Voronova A., Jansons Ā., Ruņģis D. Expression of retrotransposon-like sequences in Scots pine (Pinus sylvestris) in response to heat stress. Environ. Exp. Biol., 2011, vol. 9, pp. 121-127.

51. Kovalchuk I., Molinier J., Yao Y., Arkhipov A., Kovalchuk O. Transcriptome analysis reveals fundamental differences in plant response to acute and chronic exposure to ionizing radiation. Mutat. Res., 2007, vol. 624, pp. 101-113.

52. Jan S., Parween T., Siddiqi T.O., Mahmooduzzafar. Antioxidant modulation in response to gamma radiation induced oxidative stress in developing seedlings of Psoralea corylifolia L. J. Environ. Radioact., 2012, vol. 113, pp. 142-149.

53. Shimalina N.S., Orekhova N.A., Pozolotina V.N. Features of prooxidant and antioxidant systems of greater plantain Plantago major growing for a long time under conditions of radioactive contamination. Russian Journal of Ecology, 2018, vol. 49, pp. 375-383.

54. Kozlov M.V., Niemela P., Junttila J. Needle fluctuating asymmetry is a sensitive indicator of pollution impact on Scots pine (Pinus sylvestris). Ecol. Indic., 2002, vol. 1, pp. 271-277.

55. Møller A.P. Developmental instability of plants and radiation from Chernobyl. Oikos., 1998, vol. 81, pp. 444-448.

56. Oleksyk T.K., Novak J.M., Purdue J.R., Gashchak S.P., Smith M.H. High levels of fluctuating asymmetry in populations of Apodemus flavicollis from the most contaminated areas in Chornobyl. J. Environ. Radioact., 2004, vol. 73, pp. 1-20.

57. Makarenko E.S., Oudalova A.A., Geras’kin S.A. Morphometric measurements of Scots pine needles from radioactively contaminated area. In: XIII International Youth Scientific and Practical Conference “Future of atomic energy – AtomFuture 2017”, KnE Engineering, 2017, pp. 8-13.

58. Kashparova E., Levchuk S., Morozova V., Kashparov V. A dose rate causes no fluctuating asymmetry indexes changes in silver birch (Betula pendula (L.) Roath.) leaves and Scots pine (Pinus sylvestris L.) needles in the Chernobyl Exclusion Zone. J. Environ. Radioact., in press.

59. Fedotov I.S., Kalchenko V.A., Igonina E.V., Rubanovich A.V. Radiation and genetic consequences of ionizing irradiation on population of Pinus sylvestris L. within the zone of the Chernobyl NPP. Radiatsionnaya biologiya. Radioekologiya – Radiation Biology. Radioecology, 2006, vol. 46, pp. 268-278. (In Russian).

60. Ipatyev V., Bulavik I., Braginsky V., Goncharenko G., Dvornik A. Forest and Chernobyl: forest ecosystems after the Chernobyl nuclear power plant accident: 1986-1994. J. Environ. Radioact., 1999, vol. 42, pp. 9-38. (In Russian).

61. Kalchenko V.A., Spirin D.A. Genetics effects revealed in populations of Pinus sylvestris L. growing under exposure to small doses of chronic irradiation. Genetika – Russian Journal of Genetics, 1989, vol. 25, no. 6, pp. 1059-1064.

Full-text article (in Russian)