Abstract
Ionizing radiation directly and indirectly affects gene expression within the plant genome. To access the antioxidant response of rice to different types of ionizing radiation, rice seeds were exposed to gamma-ray, cosmic-ray and ion beam radiation. Exposure to ionizing radiation dramatically decreased the shoot length in all plants but not the root length compared with a non-irradiated plant. Electron spin resonance, confirmed that the number of free radicals in cell was greatly increased by different types of ionizing radiation. The measurement of the MDA, chlorophyll, carotenoids contents and activity of antioxidant enzymes revealed that gamma-ray and cosmic-ray, but not ion beam, ionization deceased chlorophyll and carotenoids contents, while all three ionization treatments increased the activities of peroxidase, ascorbate peroxidase, and superoxide dismutase compared with the non-irradiated plants. Microarray analysis using Affymetrix GeneChip was used to establish the gene transcript profiles of rice genes regarding ROS scavenging and signal transduction pathways after ionization treatment. Many of the rice genes involved in ROS scavenging and signal transduction pathways showed induction or repression that had increased more than twofold after ionization treatment. In particular, genes associated with electron transport, such as NADPH oxidase-like and alternative oxidase, were often down-regulated by more than twofold in response to the ionization treatments. In our transcriptomic profile analysis, we confirmed that the expression of rice genes associated with ROS scavenging and signal transduction pathways was induced or repressed to different degrees by the different types of ionizing radiations, as in other environmental stresses.
Similar content being viewed by others
Abbreviations
- APX:
-
Ascorbate peroxidase
- CAT:
-
Catalase
- DEGs:
-
Differentially expressed genes
- ESR:
-
Electron spin resonance
- GO:
-
Gene Ontology
- LET:
-
Linear energy transfer
- MDA:
-
Malonaldehyde
- MS:
-
Murashige–Skoog
- POD:
-
Peroxidase
- ROS:
-
Reactive oxygen species
- SOD:
-
Superoxide dismutase
References
Jing N, Xianghua L, Leslie MH, Lizhong X (2010) A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol 152:876–890
Felipe KT, Larissa M-B, Vinicius CG, Rogerio M, Marcia M-P (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 224:300–314
Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegem F (2000) Dual action of the oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795
Mittler R, Vanderauwera S, Gollery M, Breusegem FV (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498
Nagano AJ, Fukazawa M, Hayashi M, Ikeuchi M, Tsukaya H, Nishimura M, Hara-Nishimura I (2008) AtMap1: a DNA microarray for genomic deletion mapping in Arabidopsis thaliana. Plant J 56:1058–1065
Kovalchuk O, Burke P, Arkhipov A, Kuchma N, James SJ, Kovalchuk I, Pogribny I (2003) Genome hypermethylation in Pinus silvestris of Chernobyl—a mechanism for radiation adaptation? Mutat Res 529:13–20
Holst RW, Nagle DJ (1997) Radiation effects on plants. In: Wang W, Gorsuch JW, Hughes JS (eds) Plants for environmental studies. Lewis Publishers, Boca Raton, pp 37–81
Roldan-Arjona T, Ariza RR (2009) Repair and tolerance of oxidative DNA damage in plants. Mutat Res 681:169–179
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
Ferullo J-M, Nespoulous L, Triantaphylides C (1994) Gamma ray-induced changes in the synthesis of tomato pericarp protein. Plant Cell Environ 17:901–911
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 120:113–119
Soriano JD (1961) Mutagenic effects of gamma radiation on rice. Bot Gaz 123:57–63
Stoeva N, Zlatev Z, Bineva Z (2001) Physiological response of beans (Phaseolus vulgaris L.) to gamma-radiation contamination, II. Water-exchange, respiration and peroxidase activity. J Environ Prot Ecol 2:304–308
Zhou LB, Li WJ, Dong XC, Yu LX, Li Q, Zhou GM, Gao QX (2006) Effects of ion beam irradiation on adventitious shoot regeneration from in vitro leaf explants of Saintpaulia ionahta. Nucl Instrum Methods Phys Res B 244:349–353
Mashinsky AL, Nechitailo GS (2001) Results and prospects of studying the gravitationally sensitive systems of plants under conditions of space flight. Space Res 39:1–12
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(10):97–101
Kuang A, Musgrave ME, Matthews SW (1996) Modification of reproductive development in Arabidopsis thaliana under space-flight conditions. Planta 198:588–594
Danby K, Gehring C (2005) Engineering drought and salinity tolerance in plants: lessons from genome-wide expression profiling in Arabidopsis. Trends Biotechnol 23(11):547–552
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382
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
Abei H (1974) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 2. Academic Press, New York, pp 673–684
Pütter J (1974) Peroxidase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 2. Academic Press, New York, pp 685–690
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
Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566
Jain M, Nijhawan A, arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143:1467–1483
Wu Z, Irazarry RA, Gentleman R, Murillo FM, Spencer F (2004) A model based background adjustment for oligonucleotide expression arrays. Johns Hopkins University, Dept. of biostatistics Working Papers Paper 1
Yu X, Wu H, Wei LJ, Cheng ZL, Xin P, Huang CL, Zhabg KP, Sun YQ (2007) Characteristics of phenotype and genetic mutations in rice after spaceflight. Adv Space Res 40:528–534
Zhang BY, Wei XL, Yang FY, Zhang YW (2011) Effects of space flight factors on genetic diversity of Buchloe dactyloides seeds. Afr J Biotechnol 10(60):12812–12820
Polat M, Korkmaz M (2003) Use of electron spin resonance technique for the detection of irradiated rice seeds (Oryza sativa L.). Int J Food Sci Technol 38:653–659
Finkelstein E, Rosen GM, Rauckman EJ (1980) Spin trapping of superoxide and hydroxyl radical: practical aspects. Arch Biochem Biophys 200:1–16
Miyazaki T, Matsubara J, Matsumoto T, Khan H (1996) Reaction of metallothionein and long-lived radicals in murine liver. Radiat Phys Chem 48:293–296
Kumagai J, Katoh H, Kumada T, Tanaka A, Tano S, Miyazaki T (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 57:75–83
Kumagai J, Kumada T, Watanabe M, Miyazaki T (2000) Electron spin echo study of long-lived radicals which cause mutation in gamma-ray irradiated mammalian cells. Spectrochim Acta Part A 56:2509
Shen B, Zhuang JY, Zhang KQ, Dai WM, Lu Y, Fu LQ, Ding JM, Zheng KL (2007) QTL mapping of chlorophyll contents in rice. Agric Sci China 6(1):17–24
Liu ZQ, Liu ZY, Ma DP, Zeng SF (1984) A study on the relation between chlorophyll content and photosynthesis rate of rice. Acta Agron Sin 10:57–64 (in Chinese)
Chen WF, Xu ZJ, Zhang LB (1995) Physiological basis of super high yield breeding of rice. Liaoning Science and Technology Press, Shenyang, pp 123–150 (in Chinese)
Yang QH, Lu W, Hu ML, Wang CM, Zhang RX, Yano M, Wan JM (2003) QTL and epistatic interaction underlying leaf chlorophyll and H2O2 content variation in rice. Acta Genet Sin 30:245–250
Borzouei A, Kafi M, Khazaei H, Naseriyan B, Majdabadi A (2010) Effects of gamma radiation on germination and physiological aspects of wheat (Triticum aestivum L.) seedlings. Park J Bot 42(4):2281–2290
Jia CF, Li AL (2008) Effects of gamma radiation on mutant induction of Fagopyrum dibotrys Hara. Photosynthetica 46(3):363–369
Moleshko GI, Anton’yan AA, Sycheyev VN, Solontsova IP, Shetlik I, Doukha Y (1991) The effects of space flight factors on the pigment system of one-celled algae. USSR Space Life Sci Digest 31:43–45
Laurinavichius RA, Yaroshyus AV, Marchyukaytis A, Shvyaghdene DV, Mashinskiy AL (1986) Metabolism of pea plants grown under space flight conditions. USSR Space Sci Digest 4:23–25
Kim JH, Moon YR, Wi SG, Kim JS, Lee MH, Chung BY (2008) Differential radiation sensitivities of Arabidopsis plants at various developmental stage. Photosynthsis 24:1491–1495
Zhang X, Wu L, Yu L, Wei S, Liu J, Yu Z (2007) Effect of Ar ion beam implantation on morphological and physiological characteristics of Liquorice (Glycyrrhiza uralensis Fisch) under short-term artificial drought conditions. Plasma Sci Technol 9:235–240
Singh BB (1971) Effect of gamma-irradiation on chlorophyll content of maize leaves. Radiat Bot 11:243–244
Wang YC, Qu GZ, Li HY, Wu YJ, Wang C, Liu GF, Yang CP (2010) Enhanced salt tolerance of transgenic poplar plants expressing a manganese superoxide dismutase from Tamarix androssowii. Mol Biol Rep 37:1119–1124
Vandenhove H, Vanhoudt N, Cuypers A, Hees MV, Wannijin 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 48:778–786
Foyer CH, Noctor G (2005) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071
Lee HS, Yo SH, Kwon SY, Kim J-S, Kwak S-S (1991) Gamma radiation-induced changes of antioxidant enzymes in callus cultures of cassava (Manihot esculenta Crantz). Kor J Plant Tiss Cult 26:53–58
da Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44–57
McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055
Holmgren A (1985) Thioredoxin. Ann Rev Biochem 54:237–271
Sha S, Minakuchi K, Higaki N, Sato K, Ohtsuki K, Kurata A, Yoshikawa H, Kotaru M, Masumura T, Ichihara K, Tanaka K (1997) Purification and characterization of glutaredoxin (thioltransferase) from rice (Oryza sativa L.). J Biochem 121:842–848
Kussmaul L, Hirst J (2006) The mechanism of superoxide production by NADH:ubiquinone oxidoreductase (complex Ι) from bovine heart mitochondria. Proc Natl Acad Sci USA 103(20):7607–7612
Remacle C, Barbieri MR, Cardol P, Jamel PP (2008) Eukaryotic complex l: functional diversity and experimental systems to unravel the assembly process. Mol Genet Genomics 280:93–110
Heazlewood JL, Howell KA, Millar AH (2003) Mitochondrial complex l from Arabidopsis and rice: orthologs of mammalian and fungal components coupled with plant-specific subunits. Biochem Biophys Acta 1604(3):159–169
Fumitaka A, Koji s, Kiyoyuki M, Kinya T (2002) A single nucleotide polymorphism in the alternative oxidase gene among rice varieties differing in low temperature tolerance. FEBS Lett 527:181–185
Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96:8271–8276
Ito Y, Saisho D, Nakazono M, Tsutsumi N, Hirai A (1997) Transcript levels of tandem-arranged alternative oxidase genes in rice are increased by low temperature. Gene 203:121–129
Munnik T, Meijer HJG, Ter Riet B, Hirt H, Frank W, Bartels D, Musgrave A (2000) Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J 22:147–154
Sang Y, Cui D, Wang X (2001) Phospholipase D and phosphatidic acid-mediated generation of superoxide in Arabidopsis. Plant Physiol 126:1449–1458
Foreman J, Demidchik V, Bothwell JHF, Myiona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDJ, Davis JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446
Li HY, Chang CS, Lu LS, Liu CA, Chan MT, Charng YY (2003) Over-expression of Arabidopsis thaliana heat shock factor gene (AtHsfA1b) enhances chilling tolerance in transgenic tomato. Bot Bull Acad Sin 44:129–140
Zou J, Liu AL, Chen XB, Zhou XY, Gao GF, Wang WF, Zhang XW (2009) Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J Plant Physiol 166:851–861
Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 48:535–547
Huang J, Sun SJ, Xu DQ, Yang X, Bao YM, Wang ZF, Tang HJ, Zhang H (2009) Increased tolerance of rice to cold, drought and oxidative stresses mediated by the overexpression of a gene that encodes the zinc finger protein ZFP245. Biochem Biophys Res Commun 389:556–561
Sun SJ, Guo SQ, Bao YM, Tang HJ, Sun H, Huang J, Zhang HS (2010) Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. J Exp Bot 61(10):2807–2818
Ramamoorthy R, Jiang SY, Kumar N, Venkatesh PN, Ramachandran S (2008) A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol 49:865–879
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
Xie Z, Zhang ZL, Hanzlik S, Cook E, Shen QJ, Zhang YJ, Wang LJ (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5:1–12
Vannini C, Locatelli F, Bracale M, Magnani E, Marsoni M, Osnato M, Mattana M, Baldoni E, Caraggio I (2004) Overexpression of the rice OsMyb4 gene increases chilling and freezing tolerance of Arabidopsis thaliana plants. Plant J 37:115–127
Kim DS, Kim J-B, Goh EJ, Kim W-J, Lim 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
Acknowledgments
This work was supported by a grant from the Korea Atomic Energy Research Institute (KAERI) and the Ministry of Education, Science, and Technology (MEST), Republic of Korea.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kim, SH., Song, M., Lee, K.J. et al. 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 (2012). https://doi.org/10.1007/s11033-012-2034-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-012-2034-9