Radiation and Environmental Biophysics

, Volume 50, Issue 1, pp 1–19 | Cite as

Effects of sparsely and densely ionizing radiation on plants

  • Veronica De Micco
  • Carmen Arena
  • Diana Pignalosa
  • Marco Durante
Review

Abstract

One of the main purposes leading botanists to investigate the effects of ionizing radiations is to understand plant behaviour in space, where vegetal systems play an important role for nourishment, psychological support and functioning of life support systems. Ground-based experiments have been performed with particles of different charge and energy. Samples exposed to X- or γ-rays are often used as reference to derive the biological efficiency of different radiation qualities. Studies where biological samples are exposed directly to the space radiation environment have also been performed. The comparison of different studies has clarified how the effects observed after exposure are deeply influenced by several factors, some related to plant characteristics (e.g. species, cultivar, stage of development, tissue architecture and genome organization) and some related to radiation features (e.g. quality, dose, duration of exposure). In this review, we report main results from studies on the effect of ionizing radiations, including cosmic rays, on plants, focusing on genetic alterations, modifications of growth and reproduction and changes in biochemical pathways especially photosynthetic behaviour. Most of the data confirm what is known from animal studies: densely ionizing radiations are more efficient in inducing damages at several different levels, in comparison with sparsely ionizing radiation.

References

  1. Abe T, Matsuyama T, Sekido S, Yamaguchi I, Yoshida S, Kameya T (2002) Chlorophyll-deficient mutants of rice demonstrated that deletion of a DNA fragment by heavy-ion irradiation. J Radiat Res 43:S157–S161CrossRefGoogle Scholar
  2. Agarwal R, Rane SS, Sainis JK (2008) Effects of 60Co γ radiation on thylakoid membrane functions in Anacystis nidulans. J Photochem Photobiol B Biology 91:9–19CrossRefGoogle Scholar
  3. Al-Rubeai MAF, Godward MBE (1981) Genetic control of radiosensitivity in Phaseolus vulgaris L. J Exp Bot 21:211–216CrossRefGoogle Scholar
  4. Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plant 100:224–233CrossRefGoogle Scholar
  5. Angelini G, Ragni P, Esposito D, Giardi P, Pompili ML, Moscardelli R, Giardi MT (2001) A device to study the effect of space radiation on photosynthetic organisms. Phys Med 17:267–268Google Scholar
  6. 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 Tot Environ 157:383–386CrossRefGoogle Scholar
  7. Bayonove J, Burg M, Delpoux M, Mir A (1984) Biological changes observed on rice and biological and genetic changes observed on Tobacco after space flight in the orbital station Salyut-7 (Biobloc III experiment). Adv Space Res 4:97–101ADSCrossRefGoogle Scholar
  8. Bhaskaran S, Swaminathan MS (1960) Polyploidy and radiosensitivity in wheat and barley. Cytological and cytochemical studies. Part I. Genetica 31:449–480CrossRefGoogle Scholar
  9. Billi D, Friedmann EI, Hofer KG, Caiola MG, Ocampo-Friedmann R (2000) Ionising-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl Environ Microbiol 66:1489–1492CrossRefGoogle Scholar
  10. Bork U, Gartenbach K, Koch C, Kranz AR (1986) Biological effects of heavy ions in Arabidopsis seeds. Adv Space Res 6:149–152ADSCrossRefGoogle Scholar
  11. Bork U, Gartenbach K, Kranz AR (1989) Early and late damages induced by heavy charged particle irradiation in embryonic tissue of Arabidopsis seeds. Adv Space Res 9:117–121ADSCrossRefGoogle Scholar
  12. Britt AB (1999) Molecular genetics of DNA repair in higher plants. Trends Plant Sci 4:20–25CrossRefGoogle Scholar
  13. Cao Y, Bie T, Wang X, Chen P (2009) Induction and transmission of wheat-Haynaldia villosa chromosomal translocations. J Genet Genomics 36:313–320CrossRefGoogle Scholar
  14. Casarett AP (1968) Effects of radiation on higher plants and plant communities. Ann NY Acad Sci 59:514Google Scholar
  15. Chadwick KH, Leenhouts HP (1981) The molecular theory of radiation biology. Springer, BerlinGoogle Scholar
  16. Cheng TS, Chandlee JM (1999) The structural, biochemical, and genetic characterization of a new radiation-induced variegated leaf mutant of soybean Glycine. Proc Natl Sci Counc Repub China B 23:27–37Google Scholar
  17. Conter A, Dupouy D, Planel H (1984a) Influence of growth phase on radiation stimulation of proliferation in Synechococcus lividus in culture. Radiat Res 99:651–658CrossRefGoogle Scholar
  18. Conter A, Dupouy D, Planel H (1984b) Light modulation of radiosensitivity of Synechococcus lividus to very low doses of ionizing radiation. Environ Exp Biol 24:229–237CrossRefGoogle Scholar
  19. Cucinotta, Durante (2006) Cancer risk from exposure to galactic cosmic rays: implications for space exploration for human beings. Lancet Oncol 7:431–435CrossRefGoogle Scholar
  20. Cyranoski D (2001) Satellite will probe mutation seeds in space. Nature 410:857ADSCrossRefGoogle Scholar
  21. Davies DR (1962) The genetical control of radiosensitivity-I. Seedling characters in tomato. Heredity 17:63–74CrossRefGoogle Scholar
  22. De Micco V, Aronne G, Colla G, Fortezza R, De Pascale S (2009) Agro-biology for bioregenerative life support systems in long-term space missions: general constraints and the Italian efforts. J Pl Interact 4:241–252CrossRefGoogle Scholar
  23. De Vita VT Jr, Samuel H, Rogemberg SA (1993) Cancer, principle and practice of oncology, 4th edn. Lippincott Co, PhiladelphiaGoogle Scholar
  24. Dennis N, Ding YM (2002) Space science: science emerges from shadows of China’s space program. Nature 420:316–320ADSCrossRefGoogle Scholar
  25. Dewey WC, Miller HH, Leeper DB (1971) Chromosomal aberrations and mortality of X-irradiated mammalian cells: emphasis on repair. Proc Natl Acad Sci USA 68:667–671ADSCrossRefGoogle Scholar
  26. Dishlers VY, Rashals ID (1977) Arabidopsis. Inf Serv 14:58–61Google Scholar
  27. Durante, Cucinotta (2008) Heavy ion carcinogenesis and human space exploration. Nat Rev Cancer 8:465–472CrossRefGoogle Scholar
  28. Durante M, Kronenberg A (2005) Ground-based research with heavy ions for space radiation protection. Adv Space Res 35:180–184ADSCrossRefGoogle Scholar
  29. Durante M, Furusawa Y, George K, Gialanella G, Greco O, Grossi G, Matsufuji N, Pugliese M, Yang TC (1998) Rejoining and misrejoining of radiation-induced chromatin breaks. IV. Charged particles. Radiat Res 149:446–454CrossRefGoogle Scholar
  30. Durante M, George K, Cucinotta FA (2006) Chromosomes lacking telomeres are present in the progeny of human lymphocytes exposed to heavy ions. Radiat Res 165:51–58CrossRefGoogle Scholar
  31. Emery DA, Boardman EG, Stucker RE (1970) Some observations on the radiosentitivity of certain varietal and hybrid genotypes of cultivated peanuts (Arachis hypogaea L.). Radiat Bot 10:269–272CrossRefGoogle Scholar
  32. Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295–307Google Scholar
  33. Esposito D, Faraloni C, Margonelli A, Pace E, Torzillo G, Zanini A, Giardi MT (2006) The effect of ionising radiation on photosynthetic oxygenic microorganisms for survival in space flight revealed by automatic photosystem II-based biosensors. Z-Tec Publishing, Bremen Microgravity science technology XVIII-3/4Google Scholar
  34. Facius R, Scherer K, Reitz G, Bucker H, Nevzgodina LV, Maximova EN (1994) Particle trajectories in seeds of Lactuca sativa and chromosome aberrations after exposure to cosmic heavy ions on Cosmos Biosatellites 8 and 9. Adv Space Res 14:93–103ADSCrossRefGoogle Scholar
  35. Fenech M (2000) The in vitro micronucleus technique. Mutat Res 455:81–95Google Scholar
  36. Foreman J, Demidchik V, Bothwell JH (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 27:442–446ADSCrossRefGoogle Scholar
  37. Foyer CH, Mullineaux P (1994) Causes of photooxidative stress and amelioration of defence systems in plants. CRC Press, Boca RatonGoogle Scholar
  38. Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071CrossRefGoogle Scholar
  39. Friedberg EC (1985) DNA repair. WH Freeman and C, New YorkGoogle Scholar
  40. Galun E, Raveh D (1979) In vitro culture of tobacco protoplasts: survival of haploid and diploid protoplasts exposed to X-ray radiation at different times after isolation. Radiat Bot 15:79–82CrossRefGoogle Scholar
  41. Gardener FP, Pearce RB, Mitchell RL (1985) The physiology of crop plant, 2nd edn. Lowa State University Press, Ames, LAGoogle Scholar
  42. Gartenbach KE, Kranz AR, Zimmermann MW, Schopper E, Schott J-U, Heilmann C, Schevchenko VV (1996) Present results of the joint radiobiological ESA/IBMP experiments “seeds” aboard cosmos 2044 and 2229—correlation of micro-dosimetric data and damage endpoints in Arabidopsis thaliana plants. Adv Space Res 18:215–220ADSCrossRefGoogle Scholar
  43. Gaubin Y, Planel H, Gasset G, Pianezzi B, Clegg J, Kovalev EE, Nevzgodina LV, Maximova EN, Miller AT, Delpoux M (1983) Results on Artemia cysts, lettuce and tobacco seeds in the Biobloc 4 experiment flown aboard the Soviet Biosatellite Cosmos 1129. Adv Space Res 3:135–140ADSCrossRefGoogle Scholar
  44. George K, Durante M, Wu H, Willingham V, Cucinotta FA (2003) In vivo and in vitro measurements of complex-type chromosomal exchanges induced by heavy ions. Adv Space Res 31:1525–1535ADSCrossRefGoogle Scholar
  45. Giardi MT, Masojidek J, Godde D (1997) Discussion on the stresses affecting the turnover of the D1 reaction centre II protein. Physiol Plant 101:635–642CrossRefGoogle Scholar
  46. Glenn GM, Poovaiah BW (1990) Calcium mediated post-harvest changes in texture and cell wall structure and composition in “Golden Delicious” apples. J Am Soc Hort Sci 115:962–968Google Scholar
  47. Hagen U (1989) Radiation biology in space: a critical review. Adv Space Res 9:3–8ADSCrossRefGoogle Scholar
  48. Hammond EC, Bridgers K, Berry FD (1996) Germination, growth rates, and electron microscope analysis of tomato seeds flown on the LDEF. Radiat Meas 26:851–861CrossRefGoogle Scholar
  49. Hase Y, Shimono K, Inoue M, Tanaka A, Watanabe H (1999) Biological effects of ion beams in Nicotiana tabacum L. Radiat Environ Biophys 38:111–115CrossRefGoogle Scholar
  50. Hase Y, Yamaguchi M, Inoue M, Tanakat A (2002) Reduction of survival and induction of chromosome aberrations in tobacco irradiated by carbon ions with different linear energy transfers. Int J Radiat Biol 78:799–806CrossRefGoogle Scholar
  51. Hirono Y, Smith HH, Lyman JT, Thompson KH, Baum JW (1970) Relative biological effectiveness of heavy ions in producing mutations, tumors, and growth inhibition in the crucifer plant, Arabidopsis. Radiat Res 44:204–223CrossRefGoogle Scholar
  52. Holst RW, Nagel DJ (1997) Radiation effects on plants. In: Wang W, Gorsuch JW, Hughes JS (eds) Plants for environmental studies. Lewis Publishers, Boca Raton, FL, pp 37–81CrossRefGoogle Scholar
  53. Huang RQ, Gu RQ, Li Q (1997) Application of SSNTDs in radiobiological investigations aboard recoverable satellites. Radiat Meas 28:451–454CrossRefGoogle Scholar
  54. Jiang X (1996) Development and prospect of space mutation breeding in China. Chinese J Space Sci 16(supp.): 77–82Google Scholar
  55. Kal’ chencko VA, Fedotov IS (2001) Genetic effects of acute and chronic ionizing irradiation on Pinus sylvestris L. inhabiting the Chernobyl meltdown area. Genetics 37:437–447Google Scholar
  56. Kalcheva VP, Dragoeva AP, Kalchev KN, Enchev DD (2009) Cytotoxic and genotoxic effects of Br-containing oxaphosphole on Allium cepa L. root tip cells and mouse bone marrow cells. Genet Mol Biol 32:389–393CrossRefGoogle Scholar
  57. Kato A, Vega JM, Han F, Lamb JC, Birchler JA (2005) Advances in plant chromosome identification and cytogenetic techniques. Curr Opin Plant Biol 8:148–154CrossRefGoogle Scholar
  58. Kiefer J, Pross HD (1999) Space radiation effects and microgravity. Mutat Res 430:299–305Google Scholar
  59. Kikuchi S, Saito Y, Ryuto H, Fukunishi N, Abe T, Tanaka H, Tsujimoto H (2009) Effects of heavy-ion beams on chromosomes of common wheat, Triticum aestivum. Mutat Res 669:63–66Google Scholar
  60. Kim J-S, Baek MH, Lee YK, Lee HY, Park YI (2004) Stimulating effect of low dose gamma-ray radiation on the growth and physiological activities of Chinese cabbage cultivars. Proceedings of the 12th international congress on photosynthesis, Brisbane 18–24 August 2001, CSIRO Publishing, doi:10.1071/SA0403244
  61. Kim J-S, Moon YR, Wi SG, Kim J-S, Lee MH, Chung BY (2008) Differential radiation sensitivities of Arabidopsis plants at various developmental stages. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Photosynthesis. Energy from the sun. Springer, The Netherlands, pp. 1491–1495Google Scholar
  62. Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267CrossRefGoogle Scholar
  63. Komai F, Shikazono N, Tanaka A (2003) Sexual modification of female spinach seeds (Spinacia oleracea L.) by irradiation with ion particles. Plant Cell Rep 21:713–717Google Scholar
  64. Kovács E, Keresztes A (2002) Effect of gamma and UV-B/C radiation on plant cells. Micron 33:199–210CrossRefGoogle Scholar
  65. Kovács E, Ball G, Nessinger A (1995) The effect of irradiation on sweet cherries. Acta Aliment 24:331–343Google Scholar
  66. Kovács E, Van Duren JP, Pitifer LA, Hoch HC, Terhune T (1997) Effect of irradiation and storage on cell wall structure of golden delicious and empire apples. Acta Aliment 26:171–190Google Scholar
  67. Kovalchuk O, Arkhipov A, Barylyak I, Karachov I, Titov V, Hohn B, Kovalchuk I (2000) Plants experiencing chronic internal exposure to ionizing radiation exhibit higher frequency of homologous recombination than acutely irradiated plants. Mutat Res 449:47–56Google Scholar
  68. Kowyama Y, Saito M, Kawase T (1987) Absence of storage effects on radiation damage after thermal neutron irradiation of dry rice seeds. Japan J Breed 37:301–310Google Scholar
  69. Kraft G (1987) Radiobiological effects of very heavy ions: inactivation, induction of chromosome aberrations and strand breaks. Nucl Sci Appl 3:1–28Google Scholar
  70. Kranz AR (1986) Genetic and physiological damage induced by cosmic radiation on dry plant seeds during space flight. Adv Space Res 6:135–138ADSCrossRefGoogle Scholar
  71. Kranz AR, Bork U (1984) Biotests for heavy ion effects and preliminary total evaluation of cosmic radiation damage in Arabidopsis seeds flown during the first mission of Spacelab on STS 9. Electronic arabidopsis information service, vol 21, http://www.arabidopsis.org/ais/1984/kranz-1984-aabnr.html
  72. Kranz AR, Gartenbach KE, Zimmermann MW (1994) Initial approach to comparative studies on the evolutionary potentials of space radiation effects in a plant system. Adv Space Res 14(10):383–388ADSCrossRefGoogle Scholar
  73. Kraus MP (1969) Resistance of blue green algae to 60Co gamma radiation. Radiat Biol 9:481–489CrossRefGoogle Scholar
  74. Krikorian AD (1998) Plants and somatic embryos in space: what have we learned? Gravit Space Biol Bull 11:5–14Google Scholar
  75. Krikorian AD (1999) Somatic embryos of daylily in space: what have we learned? Adv Space Res 23:1987–1997ADSCrossRefGoogle Scholar
  76. Kumagai J, Katoh H, Kumada T, Tanaka A, Tano S, Miyazaki (2000) Strong resistance of Arabidopsis thaliana and Raphanus sativus seeds for ionizing radiation as studied by ESR, ENDOR, ESE spectroscopy and germination measurement: effect of long-lived and super-long-lived radicals. Radiat Phys chem 57:75–83ADSCrossRefGoogle Scholar
  77. Kurimoto U, Constable JVH, Hood S, Huda A (2007) Response of Arabidopsis thaliana to ionizing radiation CP958. In: Crranja C, Leroy C, Stekl I (eds) Nuclear physics methods and accelerators in biology and medicine. American Institute of Physics, USAGoogle Scholar
  78. Kurimoto T, Constable VH, Huda A (2010) Effects of ionizing radiation exposure on Arabidopsis thaliana. Heath Phys 99(1):49–57CrossRefGoogle Scholar
  79. Leyko W, Bartosz G (2000) Membrane effects of ionizing radiation and hyperthermia. Int J Radiat Biol 49:743–770CrossRefGoogle Scholar
  80. Li Y, Liu M, Cheng Z, Sun Y (2007) Space environment induced mutations prefer to occur at polymorphic sites of rice genomes. Adv Space Res 40:523–527ADSCrossRefGoogle Scholar
  81. Liu L, Van Zanten L, Shu QY, Matuszynski M (2004) Officially released mutant varieties in China. Mutat Breed Rev 14:1–62Google Scholar
  82. Luckey TD (1980) Hormesis with ionizing radiation. CRC Press Inc, Boca RatonGoogle Scholar
  83. Luckey TD (1982) Physiological benefits from low levels of ionizing radiation. Health Phys 43(6):771–789CrossRefGoogle Scholar
  84. Magnien E, Dalschaert X, Coppola M (1981) Dose-effect relationships, r.b.e. and split-dose effects after gamma-ray and fast neutron irradiation of protoplasts from wild Nicotiana species. Int J Radiat Biol Relat Stud Phys Chem Med 40:463–474CrossRefGoogle Scholar
  85. Maity JP, Mishra D, Chakraborty A, Saha A, Santra SC, Chanda S (2005) Modulation of some quantitative and qualitative characteristics in rice (Oryza sativa L.) and mung (Phaseolus mungo L.) by ionizing radiation. Radiat Phys chem 74:391–394ADSCrossRefGoogle Scholar
  86. Manti L, Bertucci A, Gialanella G, Grossi G, Pignalosa D, Pugliese M, Scampoli P, Durante M (2007) Rearrangements in human chromosome 1 visualized by arm-specific probes in the progeny of blood lymphocytes exposed to iron ions. Adv Space Res 39: 1066–1069Google Scholar
  87. Markova M, Vyskot B (2009) New horizons of genomic in situ hybridization. Cytogenet Genome Res 126:368–375CrossRefGoogle Scholar
  88. Mei M, Deng H, Lu Y, Zhuang C, Liu Z, Qiu Q, Qiu Y, Yang TC (1994) Mutagenic effects of heavy ion radiation in plants. Adv Space Res 14:363–372ADSCrossRefGoogle Scholar
  89. Mei M, Qiu Y, Sun Y, Huang R, Zhang Q, Hong M, Ye J (1998) Morphological and molecular changes of maize plants after seeds been flown on recoverable satellite. Adv Space Res 22:1691–1697ADSCrossRefGoogle Scholar
  90. Melki M, Dahmani TH (2009) Gamma irradiation effects on durum wheat (Triticum durum Desf) under various conditions. Pak J Biol Sci 12:1531–1534CrossRefGoogle Scholar
  91. Moscone EA, Klein F, Lambrou M, Fuchs J, Schweizer D (1999) Quantitative karyotyping and dual-color FISH mapping of 5S and 18S–25S rDNA probes in the cultivated Phaseolus species (Leguminosae). Genome 42:1224–1233CrossRefGoogle Scholar
  92. 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 120:113–119CrossRefGoogle Scholar
  93. Okamura M, Yasuno N, Ohtsuka M, Tanaka A, Shikazono N, Hase Y (2003) Wide variety of flower-color and shape mutants regenerated from leaf cultures irradiated with ion beams. Nucl Instrum Methods Phys Res 206:574–578ADSCrossRefGoogle Scholar
  94. Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol 5:193–198CrossRefGoogle Scholar
  95. Ou X, Long L, Zhang Y, Xue Y, Liu J, Lin X, Liu B (2009) Spaceflight induces both transient and heritable alterations in DNA methylation and gene expression in rice (Oryza sativa L.). Mutat Res 662:44–53Google Scholar
  96. Palamine MT, Cureg RGA, Marbella LJ, Lapade AG, Domingo ZB, Deocaris CC (2005) Some biophysical changes in the chloroplasts of a Dracaena radiation-mutant. Philippine J Sci 134:121Google Scholar
  97. Pfeiffer P, Goedecke W, Obe G (2000) Mechanisms of DNA double-strand break repair and their potential to induce chromosomal aberrations. Mutagenesis 15:289–302CrossRefGoogle Scholar
  98. Pignalosa D, Bertucci A, Gialanella G, Grossi G, Manti L, Pugliese M, Scampolia P, Durante M (2008) Chromosome inter- and intrachanges detected by arm-specific DNA probes in the progeny of human lymphocytes exposed to energetic heavy ions. Radiat Res 170:458–466CrossRefGoogle Scholar
  99. Polle A (2001) Dissecting the superoxide dismutase–ascorbate peroxidase–glutathione pathway in chloroplasts by metabolic modelling. Computer simulations as a step towards flux analysis. Plant Physiol 126:445–462CrossRefGoogle Scholar
  100. Qin HL, Wang YG, Xue JM, Miao Q, Ma L, Mei T, Zhang WM, Guo W, Wang JY, Gu HY (2007) Biological effects of protons targeted to different ranges in Arabidopsis seeds. Int J Radiat Biol 83:301–308CrossRefGoogle Scholar
  101. Rea G, Esposito D, Damasso M, Serafini A, Margonelli A, Faraloni C, Torzillo G, Zanini A, Bertalan I, Johanningmeier U, Giardi M (2008) Ionizing radiation impacts photochemical quantum yield and oxygen evolution activity of photosystem II in photosynthetic microorganisms. Int J Radiat Biol 84:867–877CrossRefGoogle Scholar
  102. Real A, Sundell-Bergman S, Knowles JF, Woodhead DS, Zinger I (2004) Effects of ionising radiation exposure on plants, fish and mammals: relevant data for environmental radiation protection. J Radiol Protection 24:A123–A137ADSCrossRefGoogle Scholar
  103. Saakov VS (2003) Specific effects induced by gamma-radiation on the fine structure of the photosynthetic apparatus: evaluation of the pattern of changes in the high-order derivative spectra of a green leaf in vivo in the red spectral region. Biochem Biophys 388:22–28Google Scholar
  104. Sah NK, Pramanik S, Raychowdhuri SS (1996) Peroxidase change in barley induced by ionizing and thermal radiation. Int J Radiat Biol 96:107–111CrossRefGoogle Scholar
  105. Sax K (1963) The stimulation of plant growth by ionizing radiation. BNL-6900 technical report. Brookhaven National Lab, Upton, NYGoogle Scholar
  106. Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327–330ADSCrossRefGoogle Scholar
  107. Schubert I, Fransz PF, Fuchs J, de Jong JH (2001) Chromosome painting in plants. Methods Cell Sci 23:57–69CrossRefGoogle Scholar
  108. Schwarzacher T, Leitch AR, Bennett MD, Heslop-Harrison JS (1989) In situ localization of parental genomes in a wide hybrid. Ann Bot 64:315–324Google Scholar
  109. Shi JM, Guo JG, Li WJ, Zhang M, Huang L, Sun YQ (2010) Cytogenetic effects of low doses of energetic carbon ions on rice after exposures of dry seeds, wet seeds and seedlings. J Radiat Res 51:235–242CrossRefGoogle Scholar
  110. Shikazono N, Tanaka A, Kitayama S, Watanabe H, Tano S (2002) LET dependence of lethality in Arabidopsis thaliana irradiated by heavy ions. Radiat Environ Biophys 41:159–162Google Scholar
  111. Shikazono N, Yokota Y, Kitamura S, Suzuki C, Watanabe H, Tano S, Tanaka A (2003) Mutation rate and novel tt mutants of Arabidopsis thaliana induced by carbon ions. Genetics 163:1449–1455Google Scholar
  112. Shimono K, Shikazono N, Inoue M, Tanaka A, Watanabe H (2001) Effect of fractionated exposure to carbon ions on the frequency of chromosome aberrations in tobacco root cells. Radiat Environ Biophys 40:221–225CrossRefGoogle Scholar
  113. Sidorov VP (1994) Cytogenic effect in Pinus sylvestris needle cells as a result of the Chernobyl accident radiation biology. Radioecology 34:847–851Google Scholar
  114. Smirnov EG, Shein GP, Curo NV, Mal’tseva LN (1983) Effect of acute gamma irradiation on meadow vegetation. Russian J Ecol 6:329–332Google Scholar
  115. Smith L (1942) Hereditary susceptibility to X-ray injury in Triticum monococcum. Am J Bot 29:189–191CrossRefGoogle Scholar
  116. Sparrow AH, Schwemmer SS (1974) Correlations between nuclear characteristics, growth inhibition, and survival-curve parameters (LDn, whole plant Do and Dq) for whole-plant acute gamma-irradiation of herbaceous species. Int J Radiat Biol Relat Stud Phys Chem Med 25:565–581CrossRefGoogle Scholar
  117. Sparrow AH, Schwemmer SS, Klug EE, Puglielli L (1970) Woody plants: changes in survival in response to long term (8 years) chronic gamma irradiation. Science 10:1082–1084ADSCrossRefGoogle Scholar
  118. Stoilov M, Jansson G, Eriksson G, Ehrenberg L (1966) Genetical and physiological causes of the variation of radiosensitivity in barley and maize. Radiat Bot 6:457–467CrossRefGoogle Scholar
  119. Strydom GJ, Staden JV, Smith MT (1991) The effect of gamma radiation on the ultrastructure of the peel of banana fruits. Environ Bot 31:43–49CrossRefGoogle Scholar
  120. Takagi Y (1969) The second type of gamma sensitive gene RS2 in soybean Glycine max (L.) Merrill. Gamma Field Symp 8:83–94Google Scholar
  121. Takatsuji T, Takayanagi H, Morishita K, Nojima K, Furusawa Y, Nakazawa Y, Matsuse M, Akamatsu S, Hirano N, Hirashima N, Hotokezaka S, Ijichi T, Kakimoto C, Kanemaru T, Koshitake M, Moriuchi A, Yamamoto K, Yoshikawa I (2010) Induction of micronuclei in germinating onion seed root tip cells irradiated with high energy heavy ions. J Radiat Res 51:315–323CrossRefGoogle Scholar
  122. Tanaka A, Shikazono N, Yokota Y, Watanabe H, Tano S (1997) Effects of heavy ions on the germination and survival of Arabiopsis thaliana. Int J Radiat Biol 72:121–127CrossRefGoogle Scholar
  123. Tanaka A, Kobayashi Y, Hase Y, Watanabe H (2002) Positional effect of cell inactivation on root gravitropism using heavy-ion microbeams. J Exp Bot 53(369):683–687CrossRefGoogle Scholar
  124. Tanaka A, Shikazono N, Hase Y (2010) Studies on biological effects of ion beams on lethality, molecular nature of mutation, mutation rate, and spectrum of mutation phenotype for mutation breeding in higher plants. J Radiat Res 51:223–233CrossRefGoogle Scholar
  125. Thiede ME, Link SO, Fellows RJ, Beedlow PA (1995) Effects of gamma radiation on stem diameter growth, carbon gain biomass partitioning in Helianthus annuus. Env Exp Bot 35(1):33–41CrossRefGoogle Scholar
  126. Ukai Y, Yamashita A (1969) Varietal differences in radiosensitivity with special reference to different aspects with different crops. Gamma Field Symp 8:69–81Google Scholar
  127. Vasilenko A, Sidorenko PG (1995) Induction of micronuclei in plant cells after exposure to accelerated ion irradiation. Radiat Environ Biophys 34:107–112CrossRefGoogle Scholar
  128. Vlasyuk PA (1964) Effects of ionizing radiation on the physiological-biochemical properties and metabolism of agricultural plants. Fiziologov Biokhimikov Rast. Moldavii Akad Nauk Moldavsk 1964:24–31Google Scholar
  129. Wareing PF, Phillips IJ (1981) Growth and differentiation in plants, XI. Pergamon Press, OxfordGoogle Scholar
  130. Wei Z, Liu Y, Wang G, Chen X, Li H, Yang H, Wang L, Gao Q, Wang C, Wang Y (1995) Biological effects of carbon ions with medium energy on plant seeds. Radiat Res 141:342–344CrossRefGoogle Scholar
  131. Wei LJ, Yang Q, Xia HM, Furusawa Y, Guan SH, Xin P, Sun YQ (2006) Analysis of cytogenetic damage in rice seeds induced by energetic heavy ions on-ground and after spaceflight. J Radiat Res 47:273–278CrossRefGoogle Scholar
  132. Werry PA, Stoffelsen KM (1979) The effect of ionizing radiation on the survival of free plant cells cultivated in suspension cultures. Int J Radiat Biol Relat Stud Phys Chem Med 35:293–298CrossRefGoogle Scholar
  133. Weyrather WK, Ritter S, Scholz M, Kraft G (1999) RBE for carbon track-segment irradiation in cell lines of differing repair capacity. Int J Radiat Biol 75:1357–1364CrossRefGoogle Scholar
  134. Wheeler RM, Mackowiak CL, Stutte GW, Sager JC, Yorio NC, Ruffe LM, Fortson RE, Dreschel TW, Knott WM, Corey KA (1996) NASA’s biomass production chamber: a testbed for bioregenerative life support studies. Adv Space Res 18:215–224ADSCrossRefGoogle Scholar
  135. Williams DR (2002) Isolation and integrated testing: an introduction to the Lunar-Mars life support test project. In: Lane HW, Sauer RL, Feeback DL (eds) Isolation—NASA experiments in closed-environment living, science and technology series, vol 104. Univelt Incorporated, San Diego, pp 1–6Google Scholar
  136. Wu L, Yu Z (2001) Radiobiological effects of a low-energy ion beam on wheat. Radiat Environ Biophys 40:53–57CrossRefGoogle Scholar
  137. Wu H, George K, Kawata T, Willingham V, Cucinotta FA (2001) Comparisons of F ratios generated from interphase and metaphase chromosome damage induced by high doses of low- and high-LET radiation. Radiat Res 155:57–62CrossRefGoogle Scholar
  138. Xu J, Wang J, Wei L, Li Z, Sun Y (2004) Inheritance of induction radiation sensitivity of space flight environments and γ-radiation on rice. 35th COSPAR scientific assembly. 18–25 July, Paris, FranceGoogle Scholar
  139. Yamaguchi H, Nagatomi S, Morishita T, Degi K, Tanaka A, Shikazono N, Hase Y (2003) Mutation induced with ion beam irradiation in rose. Nucl Instrum Methods Phys Res B 206:561–564ADSCrossRefGoogle Scholar
  140. Yang G, Wu L, Chen L, Pei B, Wang Y, Zhan F, Wu Y, Yu Z (2007) Targeted irradiation of shoot apical meristem of Arabidopsis embryos induces long-distance bystander/abscopal effects. Radiat Res 167:298–305CrossRefGoogle Scholar
  141. Yokota Y, Hase Y, Shikazono N, Tanaka A, Inoue M (2003) LET dependence of lethality of carbon ion irradiation to single tobacco cells. Int J Radiat Biol 79:681–685CrossRefGoogle Scholar
  142. Yokota Y, Yamada S, Hase Y, Shikazono N, Narumi I, Tanaka A, Inoue M (2007) Initial yields of DNA double-strand breaks and DNA Fragmentation patterns depend on linear energy transfer in tobacco BY-2 protoplasts irradiated with helium, carbon and neon ions. Radiat Res 167:94–101CrossRefGoogle Scholar
  143. Yu Z (2000) Ion beam application in genetic modification. IEEE Trans Plasma Sci 28:128–132ADSCrossRefGoogle Scholar
  144. Yu X, Wu H, Wei LJ, Cheng Zl, Xin P, Huang Cl, Zhang KP, Sun YQ (2007) Characteristics of phenotype and genetic mutations in rice after spaceflight. Adv Space Res 40:528–534ADSCrossRefGoogle Scholar
  145. Zaka R, Vendecasteele CM, Misset MT (2002) Effects of low chronic doses of ionizing radiation on antioxidant enzymes and G6PDH activities in Stipa capillata (Poaceae). J Exp Bot 53:1979–1987CrossRefGoogle Scholar
  146. Zhou L, Li LiWenjian, Lixia Yu, Li P, Li Q, Shuang MA, Dong X, Zhou G, Leloup C (2006) Linear energy transfer dependence of the effects of carbon ion beams on adventitious shoot regeneration from in vitro leaf explants of Saintpaulia ionahta. Int J Radiat Bio 82(7):473–481CrossRefGoogle Scholar
  147. Zimmermann MW, Gartenbach KE, Kranz AR, Baican B, Schopper E, Heilmann C, Reitz G (1996) Recent results of comparative radiobiological experiments with short and long term expositions of Arabidopsis seed embryos. Adv Space Res 18(12):205–213ADSCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Veronica De Micco
    • 1
  • Carmen Arena
    • 2
  • Diana Pignalosa
    • 3
  • Marco Durante
    • 3
    • 4
  1. 1.Dipartimento di Arboricoltura, Botanica e Patologia VegetaleUniversità degli Studi di Napoli Federico IIPortici (Naples)Italy
  2. 2.Dipartimento di Biologia Strutturale e FunzionaleUniversità degli Studi di Napoli Federico IINaplesItaly
  3. 3.Department of BiophysicsGSI Helmholtzzentrum für SchwerionenforschungDarmstadtGermany
  4. 4.Institut für Festkörperphysik, Technische Universität DarmstadtDarmstadtGermany

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