Abstract
Rates of lipid peroxidation (LPX) and protein carbonylation levels under oxidative stress in plants with different tolerance to oxygen deficiency were studied. Rice and wheat seedlings were subjected to 24 h of anoxia followed by reexposure to normoxic conditions or treated with H2O2 and generators of reactive oxygen species (ROS) such as methyl viologen, menadione, and a mixture of Cu2+ and ascorbate. Measuring thiobarbituric acid reactive substances (TBARS), we showed that more severe LPX occurs in wheat under stress conditions compared to hypoxia-tolerant rice. However, in rice roots the initial concentration of TBARS was higher than in wheat. Post-anoxia also induced protein carbonylation in both plants but it was significantly higher in wheat seedlings. Immunoblotting analysis of carbonylation level revealed that protein damage caused by reaeration was more severe compared to the effects of oxidative agents in wheat. Generally, anoxia caused most LPX in plant shoots while protein carbonylation was more pronounced in the roots. LPX and protein carbonylation were reduced in rice after 24 h reaeration while wheat failed to decrease the level of oxidative modifications to the initial values during prolonged post-anoxia.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anjum NA, Sofo A, Scopa A, Roychoudhury A, Gill SS, Iqbal M, Lukatkin AS, Pereira E, Duarte AC, Ahmad I (2015) Lipids and proteins—major targets of oxidative modifications in abiotic stressed plants. Environ Sci Pollut Res 22:4099–4121. https://doi.org/10.1007/s11356-014-3917-1
Bailey-Serres J, Lee SC, Brinton E (2012) Waterproofing crops: effective flooding survival strategies. Plant Physiol 160:1698–1709. https://doi.org/10.1104/pp.112.208173
Bhoomika K, Pyngrope S, Dubey RS (2014) Effect of aluminum on protein oxidation, non-protein thiols and protease activity in seedlings of rice cultivars differing in aluminum tolerance. J Plant Physiol 171:497–508. https://doi.org/10.1016/j.jplph.2013.12.009
Biemelt S, Keetman U, Albrecht G (1998) Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. Plant Physiol 116:651–658. https://doi.org/10.1104/pp.116.2.651
Blokhina OB, Fagerstedt KV, Chirkova TV (1999) Relationships between lipid peroxidation and anoxia tolerance in a range of species during post-anoxic reaeration. Physiol Plant 105:625–632. https://doi.org/10.1034/j.1399-3054.1999.105405.x
Blokhina O, Virolainen E, Fagerstedt KV, Hoikkala A, Wähälä K, Chirkova TV (2000) Antioxidant status of anoxia-tolerant and -intolerant plant species under anoxia and reaeration. Physiol Plant 109:396–403. https://doi.org/10.1034/j.1399-3054.2000.100405.x
Blokhina OB, Chirkova TV, Fagerstedt KV (2001) Anoxic stress leads to hydrogen peroxide formation in plant cells. J Exp Bot 52:1179–1190. https://doi.org/10.1093/jxb/52.359.1179
Chirkova T, Yemelyanov V (2018) The study of plant adaptation to oxygen deficiency in Saint Petersburg University. Biol. Commun. 63:17–31. https://doi.org/10.21638/spbu03.2018.104
Chirkova T, Novitskaya L, Blokhina O (1998) Lipid peroxidation and antioxidant systems under anoxia in plants differing in their tolerance to oxygen deficiency. Russ J Plant Physiol 45:55–62
Ciacka K, Tymiński M, Gniazdowska A, Krasuska U (2020) Carbonylation of proteins-an element of plant ageing. Planta 252:12. https://doi.org/10.1007/s00425-020-03414-1
Crawford RMM, Walton JC, Wollenweberratzer B (1994) Similarities between postischemic injury to animal-tissues and postanoxic injury in plants. Proc. R Soc Edinburgh Sect B- Biol Sci 102:325–332. https://doi.org/10.1017/S0269727000014317
Da-Silva C, Amarante L (2020) Time-course biochemical analyses of soybean plants during waterlogging and reoxygenation. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2020.104242
Demarest TG, Schuh RA, Waddell J, McKenna MC, Fiskum G (2016) Sex-dependent mitochondrial respiratory impairment and oxidative stress in a rat model of neonatal hypoxic-ischemic encephalopathy. J Neurochem 137:714–729. https://doi.org/10.1111/jnc.13590
Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM (2003) Free oxygen radicals regulate plasma membrane Ca2+- and K+-permeable channels in plant root cells. J Cell Sci 116:81–88. https://doi.org/10.1242/jcs.00201
Demiral T, Türkan İ (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53:247–257. https://doi.org/10.1016/j.envexpbot.2004.03.017
Devanathan S, Erban A, Perez-Torres R, Kopka J, Makaroff CA (2014) Arabidopsis thaliana glyoxalase 2–1 is required during abiotic stress but is not essential under normal plant growth. PLoS One. https://doi.org/10.1371/journal.pone.0095971
Dirmeier R, O’Brien KM, Engle M, Dodd A, Spears E, Poyton RO (2002) Exposure of yeast cells to anoxia induces transient oxidative stress: implications for the induction of hypoxic genes. J Biol Chem 277:34773–34784. https://doi.org/10.1074/jbc.M203902200
Ellis MH, Dennis ES, Peacock WJ (1999) Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance. Plant Physiol 119:57–64. https://doi.org/10.1104/pp.119.1.57
Goggin DE, Colmer TD (2005) Intermittent anoxia induces oxidative stress in wheat seminal roots: assessment of the antioxidant defence system, lipid peroxidation and tissue solutes. Funct Plant Biol 32:495–506. https://doi.org/10.1071/FP04194
Herzog M, Fukao T, Winkel A, Konnerup D, Lamichhane S, Alpuerto JB, Hasler-Sheetal H, Pedersen O (2018) Physiology, gene expression, and metabolome of two wheat cultivars with contrasting submergence tolerance. Plant Cell Environ 41:1632–1644. https://doi.org/10.1111/pce.13211
Hsu CH, Hsu YT (2019) Biochemical responses of rice roots to cold stress. Bot Stud 60:14. https://doi.org/10.1186/s40529-019-0262-1
Hunter MIS, Hetherington AM, Crawford RMM (1983) Lipid peroxidation-a factor in anoxia intolerance in Iris species? Phytochemistry 22:1145–1147. https://doi.org/10.1016/0031-9422(83)80209-X
Ivanina AV, Sokolova IM (2016) Effects of intermittent hypoxia on oxidative stress and protein degradation in molluscan mitochondria. J Exp Biol 219:3794–3802. https://doi.org/10.1242/jeb.146209
Jung H-I, Kong M-S, Lee B-R, Kim T-H, Chae M-J, Lee E-J, Jung G-B, Lee C-H, Sung J-K, Kim Y-H (2019) Exogenous glutathione increases arsenic translocation into shoots and alleviates arsenic-induced oxidative stress by sustaining ascorbate-glutathione homeostasis in rice seedlings. Front Plant Sci 10:1089. https://doi.org/10.3389/fpls.2019.01089
Juszczuk IM, Tybura A, Rychter AM (2008) Protein oxidation in the leaves and roots of cucumber plants (Cucumis sativus L.), mutant MSC16 and wild type. J Plant Physiol 165:355–365. https://doi.org/10.1016/j.jplph.2007.06.021
Kalemba EM, Pukacka S (2014) Carbonylated proteins accumulated as vitality decreases during long-term storage of beech (Fagus sylvatica L.) seeds. Trees 28:503–515. https://doi.org/10.1007/s00468-013-0967-9
Krasuska U, Andrzejczak O, Staszek P, Bogatek R, Gniazdowska A (2016) Canavanine alters ROS/RNS level and leads to post-translational modification of proteins in roots of tomato seedlings. Front Plant Sci 7:840. https://doi.org/10.3389/fpls.2016.00840
Kumutha D, Ezhilmathi K, Sairam RK, Srivastava GC, Deshmukh PS, Meena RC (2009) Waterlogging induced oxidative stress and antioxidant activity in pigeonpea genotypes. Biol Plant 53:75–84. https://doi.org/10.1007/s10535-009-0011-5
Levine RL, Williams JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357. https://doi.org/10.1016/s0076-6879(94)33040-9
Lounifi I, Arc E, Molassiotis A, Job D, Rajjou L, Tanou G (2013) Interplay between protein carbonylation and nitrosylation in plants. Proteomics 13:568–578. https://doi.org/10.1002/pmic.201200304
Mano J, Miyatake F, Hiraoka E, Tamoi M (2009) Evaluation of the toxicity of stress-related aldehydes to photosynthesis in chloroplasts. Planta 230:639–648. https://doi.org/10.1007/s00425-009-0964-9
Mano J, Nagata M, Okamura S, Shiraya T, Mitsui T (2014) Identification of oxidatively modified proteins in salt-stressed Arabidopsis: a carbonyl-targeted proteomics approach. Plant Cell Physiol 55:1233–1244. https://doi.org/10.1093/pcp/pcu072
Pang N, Zhang F (2015) Hypoxia-induced programmed cell death in root-tip meristematic cells of Triticum aestivum L. Acta Biol Cracoviensia Ser Bot 57:51–61. https://doi.org/10.1515/abcsb-2015-0004
Park JS, Lee EJ (2019) Waterlogging induced oxidative stress and the mortality of the Antarctic plant Deschampsia Antarctica. J ECol Environ 43:29. https://doi.org/10.1186/s41610-019-0127-2
Pavelic D, Arpagaus S, Rawyler A, Brändle R (2000) Impact of post-anoxia stress on membrane lipids of anoxia-pretreated potato cells. A re-appraisal. Plant Physiol 124:1285–1292. https://doi.org/10.1104/pp.124.3.1285
Pena LB, Barcia RA, Azpilicueta CE, Méndez AAE, Gallego SM (2012) Oxidative post translational modifications of proteins related to cell cycle are involved in cadmium toxicity in wheat seedlings. Plant Sci 196:1–7. https://doi.org/10.1016/j.plantsci.2012.07.008
Pfister-Sieber M, Brändle R (1994) Aspects of plant behaviour under anoxia and post-anoxia. Proc r Soc Edinburgh Sect B Biol Sci 102:313–324. https://doi.org/10.1017/S0269727000014305
Pompeiano A, Huarancca Reyes T, Moles TM, Villani M, Volterrani M, Guglielminetti L, Scartazza A (2017) Inter- and intraspecific variability in physiological traits and post-anoxia recovery of photosynthetic efficiency in grasses under oxygen deprivation. Physiol Plant 161:385–399. https://doi.org/10.1111/ppl.12608
Radić S, Radić-Stojković M, Pevalek-Kozlina B (2006) Influence of NaCl and mannitol on peroxidase activity and lipid peroxidation in Centaurea ragusina L. roots and shoots. J Plant Physiol 163:1284–1292. https://doi.org/10.1016/j.jplph.2005.08.019
Rubin BA, Merzlyak MN, Juferova SG (1976) Oxidation of lipid components in isolated chloroplasts under lighting. The substrates and products of lipid peroxidation. Plant Physiol Biochem 23:254–261
Santosa IE, Ram PC, Boamfa EI, Laarhoven LJJ, Reuss J, Jackson MB, Harren FJM (2007) Patterns of peroxidative ethane emission from submerged rice seedlings indicate that damage from reactive oxygen species takes place during submergence and is not necessarily a post-anoxic phenomenon. Planta 226:193–202. https://doi.org/10.1007/s00425-006-0457-z
Setter TL, Bhekasut P, Greenway H (2010) Desiccation of leaves after de-submergence is one cause for intolerance to complete submergence of the rice cultivar IR 42. Funct Plant Biol 37:1096–1104. https://doi.org/10.1071/FP10025
Shikov AE, Chirkova TV, Yemelyanov VV (2020) Post-anoxia in plants: reasons, consequences, and possible mechanisms. Russ J Plant Physiol 67:45–59. https://doi.org/10.1134/S1021443720010203
Skutnik M, Rychter AM (2009) Differential response of antioxidant systems in leaves and roots of barley subjected to anoxia and post-anoxia. J Plant Physiol 166:926–937. https://doi.org/10.1016/j.jplph.2008.11.010
Smirnoff N (1995) Antioxidant Systems and Plant Response to the Environment. In: Smirnoff V (ed) Environment and Plant Metabolism: Flexibility and Acclimation. Bios Scientific Publishers, Oxford, pp 217–243
Song H, Xu X, Wang H, Tao Y (2011) Protein carbonylation in barley seedling roots caused by aluminum and proton toxicity is suppressed by salicylic acid. Russ J Plant Physiol 58:653–659. https://doi.org/10.1134/S1021443711040169
Srivastava RK, Pandey P, Rajpoot R, Rani A, Dubey RS (2014) Cadmium and lead interactive effects on oxidative stress and antioxidative responses in rice seedlings. Protoplasma 251:1047–1065. https://doi.org/10.1007/s00709-014-0614-3
Sugiura K, Koike S, Suzuki T, Ogasawara Y (2021) Carbonylation of skin collagen induced by reaction with methylglyoxal. Biochem Biophys Res Commun 562:100–104. https://doi.org/10.1016/j.bbrc.2021.05.044
Sweetlove LJ, Møller IM (2009) Oxidation of proteins in plants-mechanisms and consequences. Adv Bot Res 52:1–23. https://doi.org/10.1016/S0065-2296(10)52001-9
Tamang BG, Fukao T (2015) Plant adaptation to multiple stresses during submergence and following desubmergence. Int J Mol Sci 16:30164–30180. https://doi.org/10.3390/ijms161226226
Tola AJ, Jaballi A, Missihoun TD (2021) Protein carbonylation: emerging roles in plant redox biology and future prospects. Plants. https://doi.org/10.3390/plants10071451
Van Toai TT, Bolles CS (1991) Postanoxic injury in soybean (Glycine max) seedlings. Plant Physiol 97:588–592. https://doi.org/10.1104/pp.97.2.588
Zuckermann H, Harren FJM, Reuss J, Parker DH (1997) Dynamics of acetaldehyde production during anoxia and post- anoxia in red bell pepper studied by photoacoustic techniques. Plant Physiol 113:925–932
Acknowledgements
The research was performed using the equipment of the Center for Molecular and Cell Technologies, St. Petersburg State University Research Park.
Funding
The article was made with the support of the Ministry of Science and Higher Education of the Russian Federation in accordance with agreement № 075-15-2020-920, date November 16, 2020, on providing a grant in the form of subsidies from the Federal budget of the Russian Federation. The grant was provided for state support for the creation and development of a World-class Scientific Center “Agrotechnologies for the Future”.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no competing interests to declare that are relevant to the content of this article.
Additional information
Communicated by R. Beckett.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Shikov, A.E., Lastochkin, V.V., Chirkova, T.V. et al. Post-anoxic oxidative injury is more severe than oxidative stress induced by chemical agents in wheat and rice plants. Acta Physiol Plant 44, 90 (2022). https://doi.org/10.1007/s11738-022-03429-z
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-022-03429-z