Plant acclimation to ionising radiation requires activation of a detoxification pathway against carbonyl-containing lipid oxidation products.
TGAII transcription factor
detoxification
lipid peroxidation
reactive carbonyl species
spontaneous chemiluminescence
ultraweak photon emission
γ radiation
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
03 Jun 2024
03 Jun 2024
Historique:
revised:
21
05
2024
received:
15
01
2024
accepted:
23
05
2024
medline:
4
6
2024
pubmed:
4
6
2024
entrez:
4
6
2024
Statut:
aheadofprint
Résumé
Ionising γ radiation produces reactive oxygen species by water radiolysis, providing an interesting model approach for studying oxidative stress in plants. Three-week old plants of Arabidopsis thaliana were exposed to a low dose rate (25 mGy h
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Electricité de France
Organisme : Commissariat à l'Énergie Atomique et aux Énergies Alternatives
Informations de copyright
© 2024 The Author(s). Plant, Cell & Environment published by John Wiley & Sons Ltd.
Références
Alméras, E., Stolz, S., Vollenweider, S., Reymond, P., Mène‐Saffrané, L. & Farmer, E.E. (2003) Reactive electrophile species activate defense gene expression in Arabidopsis. The Plant Journal, 34, 205–216.
Barjaktarovic, Z., Shyla, A., Azimzadeh, O., Schulz, S., Haagen, J., Dörr, W. et al. (2013) Ionising radiation induces persistent alterations in the cardiac mitochondrial function of C57BL/6 mice 40 weeks after local heart exposure. Radiotherapy and Oncology, 106, 404–410.
Biermans, G., Horemans, N., Vanhoudt, N., Vandenhove, H., Saenen, E., Van Hees, M. et al. (2015) Arabidopsis thaliana seedlings show an age‐dependent response on growth and DNA repair after exposure to chronic γ‐radiation. Environmental and Experimental Botany, 109, 122–130.
Birtic, S., Ksas, B., Genty, B., Mueller, M.J., Triantaphylidès, C. & Havaux, M. (2011) Using spontaneous photon emission to image lipid oxidation patterns in plant tissues. The Plant Journal, 67, 1103–1115.
Biswas, M.S. & Mano, J. (2021) Lipid peroxide‐derived reactive carbonyl species as mediators of oxidative stress and signaling. Frontiers in Plant Science, 12, 720867.
Blagojevic, D., Lee, Y., Brede, D.A., Lind, O.C., Yakovlev, I., Solhaug, K.A. et al. (2019) Comparative sensitivity to gamma radiation at the organismal, cell and DNA level in young plants of Norway spruce, Scots pine and Arabidopsis thaliana. Planta, 250, 1567–1590.
Caplin, N. & Willey, N. (2018) Ionizing radiation, higher plants, and radioprotection: from acute high doses to chronic low doses. Frontiers in Plant Science, 9, 847.
Chang, S., Lee, U., Hong, M.J., Jo, Y.D. & Kim, J.‐B. (2020) High‐throughput phenotyping (HTP) data reveal dosage effect at growth stages in Arabidopsis thaliana irradiated by gamma rays. Plants, 9, 557.
Choi, H.I., Han, S.M., Jo, Y.D., Hong, M.J., Kim, S.H. & Kim, J.‐B. (2021) Effects of acute and chronic gamma irradiation on the cell biology and physiology of rice plants. Plants, 10, 439.
Cifra, M. & Pospíšil, P. (2014) Ultra‐weak photon emission from biological samples: definition, mechanisms, properties, detection and applications. Journal of Photochemistry and Photobiology, B: Biology, 139, 2–10.
D'Alessandro, S., Mizokami, Y., Légeret, B. & Havaux, M. (2019) The apocarotenoid β‐cyclocitric acid elicits drought tolerance in plants. iScience, 19, 461–473.
D'Alessandro, S., Ksas, B. & Havaux, M. (2018) Decoding β‐cyclocitral‐mediated retrograde signaling reveals the role of a detoxification response in plant tolerance to photooxidative stress. The Plant Cell, 30, 2495–2511.
Daudi, A. & O'Brien, J. (2012) Detection of hydrogen peroxide by DAB staining in Arabidopsis Leaves. Bio‐Protocol, 2, e263.
Dowlath, M.J.H., Karuppannan, S.K., Sinha, P., Dowlath, N.S., Arunachalam, K.D., Ravindran, B. et al. (2021) Effects of radiation and role of plants in radioprotection: A critical review. Science of the Total Environment, 779, 146431.
Duarte, G.T., Volkova, P.Y., Fiengo Perez, F. & Horemans, N. (2023) Chronic ionizing radiation of plants: an evolutionary factor from direct damage to non‐target effects. Plants, 12, 1178.
Esnault, M.A., Legue, F. & Chenal, C. (2010) Ionizing radiation: advances in plant response. Environmental and Experimental Botany, 68, 231–237.
Filchenkov, G.N., Popoff, E.H. & Naumov, A.D. (2014) The low dose gamma ionising radiation impact upon cooperativity of androgen‐specific proteins. Journal of Environmental Radioactivity, 127, 182–190.
Fode, B., Siemsen, T., Thurow, C., Weigel, R. & Gatz, C. (2008) The Arabidopsis GRAS protein SCL14 interacts with class II TGA transcription factors and is essential for the activation of stress‐inducible promoters. The Plant Cell, 20, 3122–3135.
Gatz, C. (2013) From pioneers to team players: TGA transcription factors provide a molecular link between different stress pathways. Molecular Plant‐Microbe Interactions, 26, 151–159.
Havaux, M. & Ksas, B. (2022) Imaging of lipid peroxidation‐associated chemiluminescence in plants: spectral features, regulation and origin of the signal in leaves and roots. Antioxidants, 11, 1333.
Herrera‐Vásquez, A., Fonseca, A., Ugalde, J.M., Lamig, L., Seguel, A., Moyano, T.C. et al. (2021) TGA class II transcription factors are essential to restrict oxidative stress in response to UV‐B stress in Arabidopsis. Journal of Experimental Botany, 72, 1891–1905.
Horemans, N., Kariuki, J., Saenen, E., Mysara, M., Beemster, G.T.S., Sprangers, K. et al. (2023) Are Arabidopsis thaliana plants able to recover from exposure to gamma radiation? A molecular perspective. Journal of Environmental Radioactivity, 270, 107304.
Hwang, S.‐G., Lin, N.‐C., Hsiao, Y.‐Y., Kuo, C.‐H., Chang, P.‐F., Deng, W.‐L. et al. (2012) The Arabidopsis short‐chain dehydrogenase/reductase 3, an abscisic acid deficient 2 homolog, is involved in plant defense responses but not in ABA biosynthesis. Plant Physiology and Biochemistry, 51, 63–73.
IAEA (2023) What is radiation? International Atomic Energy. https://www.iaea.org/newscenter/news/what-is-radiation.
Islam, M.M., Ye, W., Matsushima, D., Rhaman, M.S., Munemasa, S., Okuma, E. et al. (2019) Reactive carbonyl species function as signal mediators downstream of H2O2 production and regulate [Ca2+]cyt elevation in ABA signal pathway in Arabidopsis guard cells. Plant and Cell Physiology, 60, 1146–1159.
Jaipo, N., Kosiwikul, M., Panpuang, N. & Prakrajang, K. (2019) Low dose gamma radiation effects on seed germination and seedling growth of cucumber and okra. Journal of Physics: Conference Series, 1380, 012106.
Kanayama, Y., Mizutani, R., Yaguchi, S., Hojo, A., Ikeda, H., Nishiyama, M. et al. (2014) Characterization of an uncharacterized aldo‐keto reductase gene from peach and its role in abiotic stress tolerance. Phytochemistry, 104, 30–36.
Kang, R., Seo, E., Kim, G., Park, A., Kim, W.J., Kang, S.‐Y. et al. (2020) Radio sensitivity of cowpea plants after gamma‐ray and proton‐beam irradiation. Plant Breeding and Biotechnology, 8, 281–292.
Kirch, H.H., Bartels, D., Wei, Y., Schnable, P.S. & Wood, A.J. (2004) The ALDH gene superfamily of Arabidopsis. Trends in Plant Science, 9, 371–377.
Kirch, H.H., Nair, A. & Bartels, D. (2001) Novel ABA‐ and dehydration‐inducible aldehyde dehydrogenase genes isolated from the resurrection plant Craterostigma plantagineum and Arabidopsis thaliana. The Plant Journal, 28, 555–567.
Kotchoni, S.O., Kuhns, C., Ditzer, A., Kirch, H.‐H. & Bartels, D. (2006) Over‐expression of different aldehyde dehydrogenase genes in Arabidopsis thaliana confers tolerance to abiotic stress and protects plants against lipid peroxidation and oxidative stress. Plant, Cell & Environment, 29, 1033–1048.
Ksas, B. & Havaux, M. (2022) Determination of ROS‐induced lipid peroxidation by HPLC‐based quantification of hydroxy polyunsaturated fatty acids. Methods in Molecular Biology, 2526, 181–189.
Kurt‐Celebi, A., Colak, N., Zeljković, S.Ć., Tarkowski, P., Zengin, A.Y. & Ayaz, F.A. (2023) Pre‐ and post‐melatonin mitigates the effect of ionizing radiation‐induced damage in wheat by modulating the antioxidant machinery. Plant Physiology and Biochemistry, 204, 108045.
LaVerne, J.A. (2000) OH radicals and oxidizing products in the gamma radiolysis of water. Radiation Research, 153, 196–200.
Mano, J., Belles‐Boix, E., Babiychuk, E., Inzé, D., Torii, Y., Hiraoka, E. et al. (2005) Protection against photooxidative injury of tobacco leaves by 2‐alkenal reductase detoxication of lipid peroxide‐derived reactive carbonyls. Plant Physiology, 139, 1773–1783.
Mano, J. & Biswas, M.S. (2018) Analysis of reactive carbonyl species generated under oxidative stress. Methods in Molecular Biology, 1743, 117–124.
Mano, J., Biswas, M.S. & Sugimoto, K. (2019) Reactive carbonyl species: a missing link in ROS signaling. Plants, 8, 391.
Mano, J., Torii, Y., Hayashi, S., Takimoto, K., Matsui, K., Nakamura, K. et al. (2002) The NADPH:Quinone oxidoreductase P1‐ζ‐crystallin in Arabidopsis catalyzes the α,β‐hydrogenation of 2‐alkenals: detoxication of the lipid peroxide‐derived reactive aldehydes. Plant & Cell Physiology, 43, 1445–1455.
De Micco, V., Arena, C., Pignalosa, D. & Durante, M. (2011) Effects of sparsely and densely ionizing radiation on plants. Radiation and Environmental Biophysics, 50, 1–19.
Moldogazieva, N.T., Zavadskiy, S.P., Astakhov, D.V. & Terentiev, A.A. (2023) Lipid peroxidation: reactive carbonyl species, protein, DNA adducts, and signaling switches in oxidative stress and cancer. Biochemical and Biophysical Research Communications, 687, 149167.
Montillet, J.‐L., Cacas, J.‐L., Garnier, L., Montané, M.‐H., Douki, T., Bessoule, J.‐J. et al. (2004) The upstream oxylipin profile of Arabidopsis thaliana: a tool to scan for oxidative stresses. The Plant Journal, 40, 439–451.
Moussa, H. (2011) Low dose of gamma irradiation enhanced drought tolerance in soybean. Acta Agronomica Hungarica, 59, 1–12.
Mueller, S., Hilbert, B., Dueckershoff, K., Roitsch, T., Krischke, M., Mueller, M.J. et al. (2008) General detoxification and stress responses are mediated by oxidized lipids through TGA transcription factors in Arabidopsis. The Plant Cell, 20, 768–785.
Munkert, J., Ernst, M., Müller‐Uri, F. & Kreis, W. (2014) Identification and stress‐induced expression of three 3β‐hydroxysteroid dehydrogenases from Erysimum crepidifolium Rchb. and their putative role in cardenolide biosynthesis. Phytochemistry, 100, 26–33.
Ning, S., Budas, G.R., Churchill, E.N., Chen, C.‐H., Knox, S.J. & Mochly‐Rosen, D. (2012) Mitigation of radiation‐induced dermatitis by activation of aldehyde dehydrogenase 2 using topical Alda‐1 in mice. Radiation Research, 178, 69–74.
Podlutskii, M., Babina, D., Podobed, M., Bondarenko, E., Bitarishvili, S., Blinova, Y. et al. (2022) Arabidopsis thaliana accessions from the Chernobyl exclusion zone show decreased sensitivity to additional acute irradiation. Plants, 11, 3142.
Prasad, A., Balukova, A. & Pospíšil, P. (2018) Triplet excited carbonyls and singlet oxygen formation during oxidative radical reaction in skin. Frontiers in Physiology, 9, 1109.
Qi, W., Zhang, L., Xu, H., Wang, L. & Jiao, Z. (2014) Physiological and molecular characterization of the enhanced salt tolerance induced by low‐dose gamma irradiation in Arabidopsis seedlings. Biochemical and Biophysical Research Communications, 450, 1010–1015.
Rac, M., Shumbe, L., Oger, C., Guy, A., Vigor, C., Ksas, B. et al. (2021) Luminescence imaging of leaf damage induced by lipid peroxidation products and its modulation by β‐cyclocitral. Physiologia Plantarum, 171, 246–259.
Restier‐Verlet, J., El‐Nachef, L., Ferlazzo, M.L., Al‐Choboq, J., Granzotto, A., Bouchet, A. et al. (2021) Radiation on earth or in space: what does it change? International Journal of Molecular Sciences, 22, 3739.
Sartorio, C., Angiolini, M., Flammini, D., Pietropaolo, A., Agostini, P., Alberghi, C. et al. (2022) Preliminary assessment of radiolysis for the cooling water system in the rotating target of SORGENTINA‐RF. Environments, 9, 106.
Semchyshyn, H.M. (2014) Reactive carbonyl species in vivo: generation and dual biological effects. The Scientific World Journal, 2014, 417842.
Shadyro, O.I., Yurkova, I.L. & Kisel, M.A. (2002) Radiation‐induced peroxidation and fragmentation of lipids in a model membrane. International Journal of Radiation Biology, 78, 211–217.
Shin, S.C., Lee, K.‐M., Kang, Y.M., Kim, K., Kim, C.S., Yang, K.H. et al. (2010) Alteration of cytokine profiles in mice exposed to chronic low‐dose ionizing radiation. Biochemical and Biophysical Research Communications, 397, 644–649.
Singh, B. & Datta, P.S. (2010) Effect of low dose gamma irradiation on plant and grain nutrition of wheat. Radiation Physics and Chemistry, 79, 819–825.
Sousa, B.C., Pitt, A.R. & Spickett, C.M. (2017) Chemistry and analysis of HNE and other prominent carbonyl‐containing lipid oxidation compounds. Free Radical Biology and Medicine, 111, 294–308.
Srinivas, U.S., Tan, B.W.Q., Vellayappan, B.A. & Jeyasekharan, A.D. (2019) ROS and the DNA damage response in cancer. Redox Biology, 25, 101084.
Sultana, M.S., Yamamoto, S., Biswas, M.S., Sakurai, C., Isoai, H. & Mano, J. (2022) Histidine‐containing dipeptides mitigate salt stress in plants by scavenging reactive carbonyl species. Journal of Agricultural and Food Chemistry, 70, 11169–11178.
Sunkar, R., Bartels, D. & Kirch, H.‐H. (2003) Overexpression of a stress‐inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. The Plant Journal, 35, 452–464.
Tang, F.R. & Loganovsky, K. (2018) Low dose or low dose rate ionizing radiation‐induced health effect in the human. Journal of Environmental Radioactivity, 192, 32–47.
Tomaž, Š., Gruden, K. & Coll, A. (2022) TGA transcription factors – structural characteristics as basis for functional variability. Frontiers in Plant Science, 13, 935819.
Triantaphylidès, C., Krischke, M., Hoeberichts, F.A., Ksas, B., Gresser, G., Havaux, M. et al. (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiology, 148, 960–968.
Turóczy, Z., Kis, P., Török, K., Cserháti, M., Lendvai, Á., Dudits, D. et al. (2011) Overproduction of a rice aldo–keto reductase increases oxidative and heat stress tolerance by malondialdehyde and methylglyoxal detoxification. Plant Molecular Biology, 75, 399–412.
UNSCEAR. (2020) Unscear 2019 Report: Source, effects and risks of ionizing radiations. New York: United Nations Publications, p. 312.
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 Physiology and Biochemistry, 48, 778–786.
Vanhoudt, N., Cuypers, A., Vangronsveld, J., Horemans, N., Wannijn, J., Van Hees, M. et al. (2011) Study of biological effects and oxidative stress related responses in gamma irradiated Arabidopsis thaliana plants. Radioprotection, 46, S401–S407.
Vanhoudt, N., Vandenhove, H., Horemans, N., Wannijn, J., Van Hees, M., Vangronsveld, J. et al. (2010) The combined effect of uranium and gamma radiation on biological responses and oxidative stress induced in Arabidopsis thaliana. Journal of Environmental Radioactivity, 101, 923–930.
Volkova, P.Y., Bondarenko, E.V. & Kazakova, E.A. (2022) Radiation hormesis in plants. Current Opinion in Toxicology, 30, 100334.
Volkova, P.Y., Geras'kin, S.A. & Kazakova, E.A. (2017) Radiation exposure in the remote period after the Chernobyl accident caused oxidative stress and genetic effects in Scots pine populations. Scientific Reports, 7, 43009.
Wang, Y., Zhao, Y., Wang, S., Liu, J., Wang, X. & Han, Y. et al. (2021) Up‐regulated 2‐alkenal reductase expression improves low‐nitrogen tolerance in maize by alleviating oxidative stress. Plant, Cell & Environment, 44, 559–573.
Weber, H., Chételat, A., Reymond, P. & Farmer, E.E. (2004) Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. The Plant Journal, 37, 877–888.
Wright, A.T., Magnaldo, T., Sontag, R.L., Anderson, L.N., Sadler, N.C., Piehowski, P.D. et al. (2015) Deficient expression of aldehyde dehydrogenase 1A1 is consistent with increased sensitivity of Gorlin syndrome patients to radiation carcinogenesis. Molecular Carcinogenesis, 54, 473–484.
Xie, L., Solhaug, K.A., Song, Y., Brede, D.A., Lind, O.C., Salbu, B. et al. (2019) Modes of action and adverse effects of gamma radiation in an aquatic macrophyte Lemna minor. Science of the Total Environment, 680, 23–34.
Yamauchi, Y., Hasegawa, A., Taninaka, A., Mizutani, M. & Sugimoto, Y. (2021) NADPH‐dependent reductases involved in the detoxification of reactive carbonyls in plants. Journal of Biological Chemistry, 286, 6999–7009.
Youn, B., Kim, S.J., Moinuddin, S.G.A., Lee, C., Bedgar, D.L., Harper, A.R. et al. (2006) Mechanistic and structural studies of apoform, binary, and ternary complexes of the Arabidopsis alkenal double bond reductase At5g16970. Journal of Biological Chemistry, 281, 40076–40088.
Yun, M., Choi, A.J., Lee, Y.C., Kong, M., Sung, J.‐Y., Kim, S.S. et al. (2018) Carbonyl reductase A is a new target to improve the effect of radiotherapy on head and neck squamous cell carcinoma. Journal of Experimental and Clinical Cancer Research, 37, 264.
Zagórski, Z.P. & Kornacka, E.M. (2012) Ionizing radiation: friend or foe of the origins of life? Origins of Life and Evolution of Biospheres, 42, 503–505.