Reactive oxygen species: Metabolism, oxidative stress, and signal transduction

Apel, Klaus; Hirt, Heribert

doi:10.1146/annurev.arplant.55.031903.141701

Cited by 11,723Plant Stress Responses and ToleranceRedox biology and oxidative stressPhotosynthetic Processes and Mechanisms

Reactive oxygen species: Metabolism, oxidative stress, and signal transduction

Apel, Klaus, Hirt, Heribert·2004·Annual Review of Plant Biology

DOI 10.1146/annurev.arplant.55.031903.141701

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Abstract

▪ Abstract Several reactive oxygen species (ROS) are continuously produced in plants as byproducts of aerobic metabolism. Depending on the nature of the ROS species, some are highly toxic and rapidly detoxified by various cellular enzymatic and nonenzymatic mechanisms. Whereas plants are surfeited with mechanisms to combat increased ROS levels during abiotic stress conditions, in other circumstances plants appear to purposefully generate ROS as signaling molecules to control various processes including pathogen defense, programmed cell death, and stomatal behavior. This review describes the mechanisms of ROS generation and removal in plants during development and under biotic and abiotic stress conditions. New insights into the complexity and roles that ROS play in plants have come from genetic analyses of ROS detoxifying and signaling mutants. Considering recent ROS-induced genome-wide expression analyses, the possible functions and mechanisms for ROS sensing and signaling in plants are compared with those in animals and yeast.

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Mechanisms of Salinity Tolerance
Munns, R., & Tester, M. (2008) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.59.032607.092911 · Cited by 13,792 · see citing works
THE ROLE OF ROOT EXUDATES IN RHIZOSPHERE INTERACTIONS WITH PLANTS AND OTHER ORGANISMS
Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S., & Vivanco, J. M. (2006) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.57.032905.105159 · Cited by 4,682 · see citing works
Reactive oxygen species homeostasis and signalling during drought and salinity stresses
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ROS Are Good
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Oxidative Stress and Neurodegenerative Diseases: A Review of Upstream and Downstream Antioxidant Therapeutic Options
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Environmentally induced oxidative stress in aquatic animals
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Mechanism of Salinity Tolerance in Plants: Physiological, Biochemical, and Molecular Characterization
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The interaction of plant biotic and abiotic stresses: from genes to the field
Atkinson, N. J., & Urwin, P. E. (2012) · Journal of Experimental Botany · doi:10.1093/jxb/ers100 · Cited by 1,880 · see citing works
Nrf2 and Oxidative Stress: A General Overview of Mechanisms and Implications in Human Disease
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Oxidative Stress in Neurodegenerative Diseases: From Molecular Mechanisms to Clinical Applications
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The role of cellular reactive oxygen species in cancer chemotherapy
Yang, H., Villani, R. M., Wang, H., Simpson, M. J., Roberts, M. S., Tang, M., & Liang, X. (2018) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-018-0909-x · Cited by 794 · see citing works
Signaling functions of phosphatidic acid
WANG, X., DEVAIAH, S., ZHANG, W., & WELTI, R. (2006) · Progress in Lipid Research · doi:10.1016/j.plipres.2006.01.005 · Cited by 757 · see citing works
Arsenic Contamination of Groundwater: A Review of Sources, Prevalence, Health Risks, and Strategies for Mitigation
Shankar, S., Shanker, U., & Shikha (2014) · The Scientific World Journal · doi:10.1155/2014/304524 · Cited by 616 · see citing works
“In addition, ROS can also act as modulators of signal transduction pathways, affecting various biological processes including cell growth, apoptosis, cell adhesion, and HIV activation [90, 91].”
Background
The contribution of environmental exposure to the etiology of autism spectrum disorder
Bölte, S., Girdler, S., & Marschik, P. B. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2988-4 · Cited by 509 · see citing works
Plant Secondary Metabolites Produced in Response to Abiotic Stresses Has Potential Application in Pharmaceutical Product Development
Yeshi, K., Crayn, D., Ritmejerytė, E., & Wangchuk, P. (2022) · Molecules · doi:10.3390/molecules27010313 · Cited by 488 · see citing works
Immune mechanisms linked to depression via oxidative stress and neuroprogression
Bakunina, N., Pariante, C. M., & Zunszain, P. A. (2015) · Immunology · doi:10.1111/imm.12443 · Cited by 444 · see citing works
Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress
Lemoine, Y., & Schoefs, B. (2010) · Photosynthesis Research · doi:10.1007/s11120-010-9583-3 · Cited by 384 · see citing works
Bright Near-Infrared Aggregation-Induced Emission Luminogens with Strong Two-Photon Absorption, Excellent Organelle Specificity, and Efficient Photodynamic Therapy Potential
Zheng, Z., Zhang, T., Liu, H., Chen, Y., Kwok, R. T. K., Ma, C., Zhang, P., Sung, H. H. Y., Williams, I. D., Lam, J. W. Y., et al. (2018) · ACS Nano · doi:10.1021/acsnano.8b03138 · Cited by 340 · see citing works
Lipid accumulation and biosynthesis genes response of the oleaginous Chlorella pyrenoidosaunder three nutrition stressors
Fan, J., Cui, Y., Wan, M., Wang, W., & Li, Y. (2014) · Biotechnology for Biofuels · doi:10.1186/1754-6834-7-17 · Cited by 341 · see citing works
Climate Change and Salinity Effects on Crops and Chemical Communication Between Plants and Plant Growth-Promoting Microorganisms Under Stress
Ullah, A., Bano, A., & Khan, N. (2021) · Frontiers in Sustainable Food Systems · doi:10.3389/fsufs.2021.618092 · Cited by 295 · see citing works
Plant salt response: Perception, signaling, and tolerance
Xiao, F., & Zhou, H. (2023) · Frontiers in Plant Science · doi:10.3389/fpls.2022.1053699 · Cited by 286 · see citing works
Traumatic stress, oxidative stress and post-traumatic stress disorder: neurodegeneration and the accelerated-aging hypothesis
Miller, M. W., & Sadeh, N. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.111 · Cited by 288 · see citing works
Abiotic Stress Signaling in Wheat—An Inclusive Overview of Hormonal Interactions During Abiotic Stress Responses in Wheat
Abhinandan, K., Skori, L., Stanic, M., Hickerson, N. M. N., Jamshed, M., & Samuel, M. A. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.00734 · Cited by 252 · see citing works
Systematic review and meta-analysis links autism and toxic metals and highlights the impact of country development status: Higher blood and erythrocyte levels for mercury and lead, and higher hair antimony, cadmium, lead, and mercury
Saghazadeh, A., & Rezaei, N. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.07.011 · Cited by 146 · see citing works
Brahmi (Bacopa monnieri): An ayurvedic herb against the Alzheimer's disease
Dubey, T., & Chinnathambi, S. (2019) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2019.108153 · Cited by 151 · see citing works
Oxidative stress biomarkers in patients with endometriosis: systematic review
Carvalho, L. F. P., Samadder, A. N., Agarwal, A., Fernandes, L. F. C., & Abrão, M. S. (2012) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-012-2439-7 · Cited by 140 · see citing works
Flux-Balance Modeling of Plant Metabolism
Sweetlove, L. J., & Ratcliffe, R. G. (2011) · Frontiers in Plant Science · doi:10.3389/fpls.2011.00038 · Cited by 137 · see citing works
Danger signals in liver injury and restoration of homeostasis
Han, H., Desert, R., Das, S., Song, Z., Athavale, D., Ge, X., & Nieto, N. (2020) · Journal of Hepatology · doi:10.1016/j.jhep.2020.04.033 · Cited by 127 · see citing works
An endophytic isolate of the fungus Yarrowia lipolytica produces metabolites that ameliorate the negative impact of salt stress on the physiology of maize
Gul Jan, F., Hamayun, M., Hussain, A., Jan, G., Iqbal, A., Khan, A., & Lee, I.-J. (2019) · BMC Microbiology · doi:10.1186/s12866-018-1374-6 · Cited by 116 · see citing works
Genome-wide association analysis of seedling traits in diverse Sorghum germplasm under thermal stress
Chopra, R., Burow, G., Burke, J. J., Gladman, N., & Xin, Z. (2017) · BMC Plant Biology · doi:10.1186/s12870-016-0966-2 · Cited by 113 · see citing works
A lycopene β-cyclase gene, IbLCYB2, enhances carotenoid contents and abiotic stress tolerance in transgenic sweetpotato
Kang, C., Zhai, H., Xue, L., Zhao, N., He, S., & Liu, Q. (2018) · Plant Science · doi:10.1016/j.plantsci.2018.05.005 · Cited by 110 · see citing works
Effective microorganisms improve growth performance, alter nutrients acquisition and induce compatible solutes accumulation in common bean (Phaseolus vulgaris L.) plants subjected to salinity stress
Talaat, N. B., Ghoniem, A. E., Abdelhamid, M. T., & Shawky, B. T. (2015) · Plant Growth Regulation · doi:10.1007/s10725-014-9952-6 · Cited by 112 · see citing works
NAD + Biosynthesis and Signaling in Plants
Gakière, B., Hao, J., de Bont, L., Pétriacq, P., Nunes-Nesi, A., & Fernie, A. R. (2018) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2018.1505591 · Cited by 108 · see citing works
Metal peroxides for cancer treatment
He, J., Fu, L.-H., Qi, C., Lin, J., & Huang, P. (2021) · Bioactive Materials · doi:10.1016/j.bioactmat.2021.01.026 · Cited by 93 · see citing works
Sulfonamides-induced oxidative stress in freshwater microalga Chlorella vulgaris: Evaluation of growth, photosynthesis, antioxidants, ultrastructure, and nucleic acids
Chen, S., Wang, L., Feng, W., Yuan, M., Li, J., Xu, H., Zheng, X., & Zhang, W. (2020) · Scientific Reports · doi:10.1038/s41598-020-65219-2 · Cited by 95 · see citing works
Alleviation of reactive oxygen species enhances PUFA accumulation in Schizochytrium sp. through regulating genes involved in lipid metabolism
Zhang, S., He, Y., Sen, B., Chen, X., Xie, Y., Keasling, J. D., & Wang, G. (2018) · Metabolic Engineering Communications · doi:10.1016/j.meteno.2018.03.002 · Cited by 90 · see citing works
Reactive Oxygen Species and Photosynthesis
Hajiboland, R. (2014) · Oxidative Damage to Plants · doi:10.1016/b978-0-12-799963-0.00001-0 · Cited by 89 · see citing works
β-Aminobutyric acid induces resistance of mango fruit to postharvest anthracnose caused by Colletotrichum gloeosporioides and enhances activity of fruit defense mechanisms
Zhang, Z., Yang, D., Yang, B., Gao, Z., Li, M., Jiang, Y., & Hu, M. (2013) · Scientia Horticulturae · doi:10.1016/j.scienta.2013.05.023 · Cited by 84 · see citing works
OsIAA18, an Aux/IAA transcription factor gene, is involved in Salt and drought tolerance in rice
Wang, F., Niu, H., Xin, D., Long, Y., Wang, G., Liu, Z., Li, G., Zhang, F., Qi, M., Ye, Y., et al. (2021) · Frontiers in Plant Science · doi:10.3389/fpls.2021.738660 · Cited by 82 · see citing works
Differential effectiveness of Serratia plymuthica IC1270-induced systemic resistance against hemibiotrophic and necrotrophic leaf pathogens in rice
De Vleesschauwer, D., Chernin, L., & Höfte, M. M. (2009) · BMC Plant Biology · doi:10.1186/1471-2229-9-9 · Cited by 77 · see citing works
DMSO triggers the generation of ROS leading to an increase in artemisinin and dihydroartemisinic acid in Artemisia annua shoot cultures
Mannan, A., Liu, C., Arsenault, P. R., Towler, M. J., Vail, D. R., Lorence, A., & Weathers, P. J. (2010) · Plant Cell Reports · doi:10.1007/s00299-009-0807-y · Cited by 75 · see citing works
Elevated p62/SQSTM1 determines the fate of autophagy-deficient neural stem cells by increasing superoxide
Wang, C., Chen, S., Yeo, S., Karsli-Uzunbas, G., White, E., Mizushima, N., Virgin, H. W., & Guan, J.-L. (2016) · Journal of Cell Biology · doi:10.1083/jcb.201507023 · Cited by 69 · see citing works
Drying Affects Artemisinin, Dihydroartemisinic Acid, Artemisinic Acid, and the Antioxidant Capacity of Artemisia annua L. Leaves
Ferreira, J. F. S., & Luthria, D. L. (2010) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf903222j · Cited by 68 · see citing works
Mechanism of artemisinin phytotoxicity action: Induction of reactive oxygen species and cell death in lettuce seedlings
Yan, Z.-Q., Wang, D.-D., Ding, L., Cui, H.-Y., Jin, H., Yang, X.-Y., Yang, J.-S., & Qin, B. (2015) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2015.01.010 · Cited by 68 · see citing works
Impact of erythromycin on a non-target organism: Cellular effects on the freshwater microalga Pseudokirchneriella subcapitata
Machado, M. D., & Soares, E. V. (2019) · Aquatic Toxicology · doi:10.1016/j.aquatox.2019.01.014 · Cited by 68 · see citing works
Abiotic Stress Responses are Governed by Reactive Oxygen Species and Age
Kanojia, A., & Dijkwel, P. P. (2018) · Annual Plant Reviews online · doi:10.1002/9781119312994.apr0611 · Cited by 64 · see citing works
Proteomic analyses of the cyanobacterium Arthrospira (Spirulina) platensis under iron and salinity stress
Ismaiel, M. M. S., Piercey-Normore, M. D., & Rampitsch, C. (2018) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2017.11.013 · Cited by 57 · see citing works
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“SOD, CAT, POD, GR, and APX are ROS-scavenging and mediate in the reaction cycle of antioxidant chemicals, including ascorbic acid (AsA) and glutathione (GSH) (Apel and Hirt, 2004; Dietz et al., 2006; Türkan and Demiral, 2009).”
Background
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Authors: Apel, K., & Hirt, H.
Affiliations: ETH Zurich (CH)
Max F. Perutz Laboratories, University of Vienna, Gregor-Mendel-Institute of Molecular Plant Sciences, Austrian Academy of Sciences, Vienna Biocenter, Dr. Bohrgasse 9, 1030 Vienna, Austria;
Venue: Annual Review of Plant Biology
Publisher: Annual Reviews
Published: 2004-06-02
Volume: 55
Issue: 1
Pages: 373-399
ISSN: 1543-5008 (ISSN-L)
1545-2123
DOI: 10.1146/annurev.arplant.55.031903.141701
OpenAlex: W2139328007
Cited by: 11,723
References: 139
Citations by year: 2026: 476 · 2025: 539 · 2024: 627 · 2023: 689 · 2022: 798 · 2021: 793 · 2020: 715 · 2019: 733 · 2018: 627 · 2017: 699 · 2016: 659 · 2015: 670 · 2014: 632 · 2013: 612 · 2012: 525
FWCI: 13.55
Type: journal article
Language: en
Open access: closed
Locations: Annual Review of Plant Biology (publishedVersion)
PubMed (publishedVersion)
Funders: European Commission
Topics: Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
Keywords: reactive oxygen species, oxidative stress, ROS signaling, reactive oxygen species scavenging, aerobic metabolism, abiotic stress, biotic stress, pathogen defense, programmed cell death, stomatal behavior, plant development
MeSH terms: Aerobiosis, Plant Diseases, Plants, Signal Transduction, Reactive Oxygen Species, Oxidative Stress, Gene Expression Regulation, Plant, Plant Physiological Phenomena

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Reactive oxygen species: Metabolism, oxidative stress, and signal transduction

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