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Physiological changes and anti-oxidative responses of Arabidopsis plants after acute and chronic γ-irradiation

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Abstract

To identify the effects of acute and chronic γ-irradiation in Arabidopsis plants, physiological responses and antioxidant-related gene expression were investigated. Seedlings were exposed to 200 Gy of γ-irradiation in acute manner for 1 or 24 h (A1 and A24) or in chronic manner for 1, 2, or 3 weeks (C1 W, C2 W, and C3 W). Plant height, silique number, and silique length in A1 and A24 irradiated plants were significantly reduced when compared to non-irradiated plants. Silique number decreased in response to both acute and chronic irradiation, except with the C3 W treatment, and the number of trichomes dramatically increased in A1 and C1 W. Electron spin resonance signal intensities increased in A1 and in all chronically irradiated plants, but decreased in the A24-treated plant. To investigate the effects of acute and chronic γ-irradiation on antioxidant enzymes, we examined activity of four antioxidant enzymes: catalase (CAT), peroxidase (POD), ascorbate peroxidase, and superoxide dismutase. In general, POD and CAT activities decreased in response to acute and chronic γ-irradiation. Oligonucleotide microarrays were used to investigate transcriptional changes after irradiation. Several genes related to reactive oxygen species signaling were up-regulated after acute and chronic exposure, including genes encoding heat shock factors, zinc finger proteins, NADPH oxidase, WRKY DNA-binding proteins, and calcium binding proteins. Taken together, our data indicate that the responses and activation of antioxidant systems prompted by irradiation exposure are dependent upon the γ-ray dose rate.

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Abbreviations

ESR:

Electron spin resonance

CAT:

Catalase

POD:

Peroxidase

APX:

Ascorbate peroxidase

SOD:

Superoxide dismutase

DSB:

Double strand break

SSB:

Single strand break

HR:

Homologous recombination

NHEJ:

Non-homologous end joining

ROS:

Reactive oxygen species

TEM:

Transmission electron microscopy

MDA:

Malondialdehyde

TCA:

Trichloroacetic acid

TBA:

Thiobarbituric acid

POBN:

α-(4-pyridyl-1-oxide)-N-tert-butylnitrone

HSF:

Heat shock factor

References

  • Abe K, Osakabe K, Ishikawa Y, Tagiri A, Yamanouchi H, Takyuu T, Yoshioka T, Ito T, Kobayashi M, Shinozaki K, Ichikawa H, Toki S (2009) Inefficient double-strand DNA break repair is associated with increased fasciation in Arabidopsis BRCA2 mutants. J Exp Bot 60:2751–2761

    Article  Google Scholar 

  • Aebi H (1974) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, New York, pp 673–684

    Chapter  Google Scholar 

  • Andre CM, Oufir M, Guignard C, Hoffmann L, Hausman J-F, Evers D, Larodelle Y (2007) Antioxidant profiling of native Andean potato tubers (Solanum tuberosum L.) reveals cultivars with high levels of β-carotene, α-tocopherol, chlorogenic anid, and petanin. J Agric Food Chem 55:10839–10849

    Article  Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72:248–254

    Article  Google Scholar 

  • Britt AB (1999) Molecular genetics of DNA repair in higher plants. Trends Plant Sci 4:20–25

    Article  Google Scholar 

  • Casarett AP (1968) Radiation chemistry and effects of gamma radiation on the cell. In: Casarett AP (ed) Radiation Biology. Prentice-Hall, Englewood Cliffs, NJ

    Google Scholar 

  • Chen L, Song Y, Li S, Ahang L, Zou C, Yu D (2012) The role of WRKY transcription factors in plant abiotic stresses. BBA-Gene Regul Mech 1819:120–128

    Google Scholar 

  • Cho YS, Lee HS, Pai HS (2000) Expression patterns of diverse genes in response to gamma irradiation in Nicotiana tabacum. J Plant Biol 43:82–87

    Article  Google Scholar 

  • de Silva AS, Danielowski R, Braga EJB, Deuner S, Magalhaes Junior AM, Peters JA (2011) Development of rice seedlings grown from pre-hydrated seeds and irradiated with gamma rays. Ciênc agrotec Lavras. 35(6):1093–1100

    Article  Google Scholar 

  • DeFalco TA, Bender KW, Snedden WA (2010) Breaking the code: Ca2+ sensors in plant signalling. Biochem J 425:27–40

    Article  Google Scholar 

  • Dhindsa RS, Matowe W (1981) Drought tolerance in two mosses: correlated with enzymatic defense against lipid peroxidation. J Exp Bot 32:79–91

    Article  Google Scholar 

  • Duboc C, Strache R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15(10):573–581

    Article  Google Scholar 

  • Edge R, McCarey DJ, Truscott TG (1997) The carotenoids as anti-oxidants: a review. J Photochem Photobiol, B 41:189–200

    Article  Google Scholar 

  • Fedotov IS, Kal’chenko VA, Igoninna EV, Rubanovich AV (2006) Irradiation and genetic consequences of ionizing irradiation on population of Pinus sylvestris L. within the zone of the Chernobyl NPP. Radiats Biol Radioecol 46:268–278

    Google Scholar 

  • Gairola S, Naidoo Y, Bhatt A, Nicholas A (2009) An investigation of the foliar trichomes of Tetradenia riparia (Hochst.) Codd [Lamiaceae]: an important medicinal plant of Southern Africa. Flora 204:325–330

    Article  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bioch 48:909–930

    Article  Google Scholar 

  • Gong Z, Koiwa H, Cushman MA, Ray A, Bufford D, Kore-eda S, Matsumoto TK, Zhu J, Cushman JC, Bressan RA, Hasegawa PM (2001) Genes that are uniquely stress regulated in salt overly sensitive (sos) mutants. Plant Physiol 126:363–375

    Article  Google Scholar 

  • Hayashi T, Aoki S (1985) Effect of irradiation on the carbohydrate metabolism responsible for sucrose accumulation in potatoes. J Agric Food Chem 33:13–17

    Google Scholar 

  • Jan S, Parween T, Siddiqi TO, Mahmooduzzafar X (2012) Effect of gamma radiation on morphological, biochemical, and physiological aspects of plants and plant products. Environ Rev 20:17–39

    Article  Google Scholar 

  • Kim JS, Kim JK, Lee EK, Lee YB (1997) Irradiation hormesis on the growth of chinese cabbage and radish. Korean J Environ Agric 16:390–393

    Google Scholar 

  • Kim J-H, Baek M-H, Chung BY, Wi SG, Kim J-S (2004) Alterations in the photosynthetic pigments and antioxidant machineries of red pepper (Capsicum annuum L.) seedlings from gamma-irradiated seeds. J Plant Biol 47:314–321

    Article  Google Scholar 

  • Kim J-H, Chung BY, Kim JS, Wi SB (2005) Effects of in planta gamma-irradiation on growth, photosynthesis, and antioxidative capacity of red pepper (Capsicum annuum L.) plants. J Plant Biol 48:47–56

    Article  Google Scholar 

  • Kim S-H, Song M, Lee KJ, Hwang S-G, Jang CS, Kim J-B, Kim SH, Ha B-K, Kang S-Y, Kim DS (2012) Genome-wide transcriptome profiling of ROS scavenging and signal transduction pathways in rice (Oryza sativa L.) in response to different types of ionizing radiation. Mol Biol Rep 39:11231–11248

    Article  Google Scholar 

  • Kimura S, Shibato J, Agrawal GK, Kim YK, Nahm BH, Jwa NS, Iwahashi H, Rakwal R (2007) Microarray analysis of rice leaf response to radioactivity from contaminated Chernobyl soil. Rice Genetics Newsletter 24:52–54

    Google Scholar 

  • Kotak S, Larkindale J, Lee U, Koskull-Döring P, Vierling E, Scharf K-D (2007) Complexity of the heat stress response in plants. Plant Biol 10:310–316

    Google Scholar 

  • Kovalchuk O, Arkhipov A, Barylyak I, Karachov I, Titov V, Hohn B, Kovalchuk I (2000) Plants experiencing chronic internal exposure to ionizing irradiation exhibit higher frequency of homologous recombination than acutely irradiated plants. Mutat Res 449:47–56

    Article  Google Scholar 

  • 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 irradiation. Mutat Res 624:101–113

    Article  Google Scholar 

  • Kumari R, Singh S, Agrawal SB (2010) Responses of ultraviolet-B induced antioxidant defense system in medicinal plant Acorus calamus L. J Environ Biol 31:907–911

    Google Scholar 

  • Lee J, Kausar T, Kim BK, Kwon JH (2008) Detection of γ-irradiated sesame seeds before and after roasting by analyzing photostimulated luminescence, thermoluminescence, and electron spin resonance. J Agric Food Chem 56:7184–7188

    Article  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids; pigments of photosynthetic biomembranes. Method Enzymol 148:350–382

    Article  Google Scholar 

  • Mahdavian K, Ghorbanli M, Kalantari KM (2008) The effects of ultraviolet radiation in the contents of chlorophyll, flavonoid, anthocyanin and proline in Capsicum annuum L. Turk J Bot 32:25–33

    Google Scholar 

  • Marc DA, Tottempudi KP, Cecil RS (1995) Changes in isozyme profiles of catalase, peroxidase and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiol 109:1247–1257

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Mittler R, Zilinskas BA (1993) Detection of ascorbate peroxidase activity in native gels by inhibition of ascorbate dependent reduction of nitroblue tetrazolium. Anal Biochem 112:540–546

    Article  Google Scholar 

  • Nagata T, Todoriski S, Hayashi T, Shibata Y, Mori M, Kanegae H, Kikuchi S (1999) γ-irradiation induces leaf trichome formation in Arabidopsis. Plant Physiol 120:113–120

    Article  Google Scholar 

  • Nagata T, Todoriki S, Masumizu T, Suda I, Furuta S, Du Z, Kikuchi S (2003) Levels of active oxygen species are controlled by ascorbic acid and anthocyanin in Arabidopsis. J Agric Food Chem 51:2992–2999

    Article  Google Scholar 

  • Nagata T, Todoriki S, Kikuchi S (2004) Radical expansion of root cells and elongation of root hairs of Arabidopsis thaliana induced by massive doses of gamma irradiation. Plant Cell Physiol 45:1557–1565

    Article  Google Scholar 

  • Nagata T, Yamada H, Du Z, Todoriki S, Kikuchi S (2005) Microarray analysis of genes that respond to gamma-irradiation in Arabidopsis. J Agric Food Chem 53:1022–1030

    Article  Google Scholar 

  • Naito K, Kusaba M, Shikazono N, Takano T, Tanaka A, Tanisaka T, Nishimura M (2005) Transmissible and nontransmissible mutations induced by irradiating Arabidopsis thaliana pollen with γ-rays and carbon ions. Genetics 169:881–889

    Article  Google Scholar 

  • Ogawa M, Uritani J (1970) Effect of gamma radiation in peroxidase development in sweet potatoes disks. Radiat Res 41(2):342–351

    Article  Google Scholar 

  • Osma MS (2002) Molecular genetic studies on irradiated wheat plants. Dissertation, University of Ain Shams

  • Park PJ, Je JY, Kim SK (2003) Free radical scavenging activity of chitooligosaccharides by electron spin resonance spectrometry. J Agric Food Chem 51:4624–4627

    Article  Google Scholar 

  • Park YD, Kim DY, Jin CH, Yang HS, Choi DS, Yook HS, Byun MW, Jeong IY (2011) Development of a method based on ESR spectroscopy for the identification of irradiated beef, pork, and chicken meats. Food Sci Biotech 20(2):367–370

    Article  Google Scholar 

  • Pütter J (1974) Peroxidase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, New York, pp 685–690

    Chapter  Google Scholar 

  • Qu A-L, Ding Y-F, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response Biochem Bioph Res Co 432:203–207

    Article  Google Scholar 

  • Rakwal R, Agrawal GK, Shibato J, Imanaka T, Fukutani S, Tamogami S, Endo S, Sahoo SK, Masuo Y, Kimura S (2009) Ultra low-dose irradiation: stress responses and impacts using rice as a grass model. Int J Mol Sci 10:1215–1225

    Article  Google Scholar 

  • Ricaud L, Proux C, Renou J-P, Pichon O, Fochesato S, Ortet P, Montané M-H (2007) ATM-mediated transcriptional and developmental response to γ-rays in Arabidopsis. PLoS ONE 2(5):e430

    Article  ADS  Google Scholar 

  • Rizhsky L, Davletova S, Liang H, Mittler R (2004) The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279:11736–11743

    Article  Google Scholar 

  • Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746

    Article  Google Scholar 

  • Scandalios JG, Tong WF, Roupakias DG (1980) Cat3, a third gene locus coding for a tissue-specific catalase in maize:genetics, intracellular location, and some biochemical properties. Mol Genet Genomics 179:33–41

    Article  Google Scholar 

  • Simmons AT, Gurr GM (2005) Trichome of Lycopersicon species and their hybrids: effects on pests and natural enemies. Agr Forest Entomol 7:265–276

    Article  Google Scholar 

  • Singh R, Singh S, Tripathi R, Lonergan P (2011) Supplemental UV-B radiation induced changes in growth, pigmants and antioxidant pool of bean (Dolichos lablab) under field conditions. J Environ Biol 32:139–145

    Google Scholar 

  • Sinha AK, Jaggi M, Raghuram B, Tuteja N (2011) Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal Behav 6(2):196–203

    Article  Google Scholar 

  • Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58

    Article  Google Scholar 

  • Sparrow AH, Christen E (1953) Tolerance of certain higher plants to chronic exposure to gamma irradiation from cobalt-60. Science 118:697–698

    Article  ADS  Google Scholar 

  • Swindell WR, Huebner M, Weber AP (2007) Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathway. BMC Genom 8:125

    Article  Google Scholar 

  • 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 Bioch 48:778–786

    Article  Google Scholar 

  • Werker E (2000) Trichome diversity and development. Adv Bot Res 31:1–35

    Article  Google Scholar 

  • Wi SG, Chung BY, Kim J-S, Kim J-H, Baek M-H, Yang DH, Lee J-W, Kim J-S (2005) Ultrastructural changes of cell organelles in Arabidopsis stems after gamma irradiation. J Plant Biol 48(2):195–200

    Article  Google Scholar 

  • Wi SG, Chung BY, Kim JS, Kim JH, Baek MH, Lee JW (2006) Localization of hydrogen peroxide in pumpkin (Cucurbita ficifolia Bouché) seedlings exposed to high dose gamma ray. J Plant Biol 49:1–8

    Article  Google Scholar 

  • 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 38:553–564

    Article  Google Scholar 

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Acknowledgments

This work was supported by grants from the Korea Atomic Energy Research Institute (KAERI) and the Nuclear R and D Program by the Ministry of Science, ICT and Future Planning (MSIP), Republic of Korea.

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Authors and Affiliations

  1. Advanced Radiation Technology Institute, Korea Atomic Energy Research Institute, 29 Geumgu, Jeongeup, Jeonbuk, 580-185, Republic of korea

    Eun Jeong Goh, Jin-Baek Kim, Sang Hoon Kim, Si–Yong Kang & Dong Sub Kim

  2. Basic Herbal Medicine Research Group, Herbal Medicine Research Division, Korea Institute of Oriental Medicine, Daejeon, 305-811, Republic of korea

    Wook-Jin Kim

  3. Division of Biotechnology and Genetic Engineering, Korea University, Anam, Seongbuk, Seoul, 136-701, Republic of korea

    Jin-Baek Kim & Yong Weon Seo

  4. Division of Plant Biotechnology, Chonnam National University, Gwangju, 500-757, Republic of korea

    Bo-Keun Ha

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  1. Eun Jeong Goh
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  2. Jin-Baek Kim
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Correspondence to Dong Sub Kim.

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Eun Jeong Goh and Jin-Baek Kim have equally contributed.

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Goh, E.J., Kim, JB., Kim, WJ. et al. Physiological changes and anti-oxidative responses of Arabidopsis plants after acute and chronic γ-irradiation. Radiat Environ Biophys 53, 677–693 (2014). https://doi.org/10.1007/s00411-014-0562-5

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