Reactive oxygen species: Connecting eustress, hormesis, and allostasis in plants

Agathokleous, 2022, On the meta-analysis of hormetic effects, Sci. Total Environ., 852, 10.1016/j.scitotenv.2022.158273 Agathokleous, 2019, Hormesis: the dose response for the 21st century: the future has arrived, Toxicology, 425, 10.1016/j.tox.2019.152249 Agathokleous, 2019, Hormesis: a compelling platform for sophisticated plant science, Trends Plant Sci., 24, 318, 10.1016/j.tplants.2019.01.004 Agathokleous, 2020, Chlorophyll hormesis: are chlorophylls major components of stress biology in higher plants?, Sci. Total Environ., 726, 10.1016/j.scitotenv.2020.138637 Agathokleous, 2020, Hormesis: highly generalizable and beyond laboratory, Trends Plant Sci., 25, 1076, 10.1016/j.tplants.2020.05.006 Antoniou, 2016, Unravelling chemical priming machinery in plants: the role of reactive oxygen-nitrogen-sulfur species in abiotic stress tolerance enhancement, Curr. Opin. Plant Biol., 33, 101, 10.1016/j.pbi.2016.06.020 Asai, 2008, MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana, Plant Cell, 20, 1390, 10.1105/tpc.107.055855 Baena-González, 2008, Convergent energy and stress signaling, Trends Plant Sci., 13, 474, 10.1016/j.tplants.2008.06.006 Banerjee, 2019, Abiotic stress tolerance in plants by priming and pretreatment with hydrogen peroxide, Prim. Pretreat. Seeds Seed., 417, 10.1007/978-981-13-8625-1_20 Baxter, 2014, ROS as key players in plant stress signalling, J. Exp. Bot., 65, 1229, 10.1093/jxb/ert375 Belz, 2014, Herbicides and plant hormesis, Pest Manag. Sci., 70, 698, 10.1002/ps.3726 Bienertova-Vasku, 2020, Eustress and distress: neither good nor bad, but rather the same?, BioEssays, 42, 10.1002/bies.201900238 Breeze, 2022, The passage of H2O2 from chloroplasts to their associated nucleus during retrograde signalling: reflections on the role of the nuclear envelope, Plants (Basel, Switzerland), 11, 552 Brossa, 2015, Redox proteomics and physiological responses in Cistus albidus shrubs subjected to long-term summer drought followed by recovery, Planta, 241, 803, 10.1007/s00425-014-2221-0 Calabrese, 2016, Preconditioning is hormesis part II: How the conditioning dose mediates protection: dose optimization within temporal and mechanistic frameworks, Pharmacol. Res., 110, 265, 10.1016/j.phrs.2015.12.020 Calabrese, 2007, Biological stress response terminology: integrating the concepts of adaptive response and preconditioning stress within a hormetic dose-response framework, Toxicol. Appl. Pharmacol., 222, 122, 10.1016/j.taap.2007.02.015 Calabrese, 2001, Hormesis: a generalizable and unifying hypothesis, Crit. Rev. Toxicol., 31, 353, 10.1080/20014091111730 Calabrese, 1999, Hormesis: a highly generalizable and reproducible phenomenon with important implications for risk assessment, 19, 261 Calabrese, 2009, Hormesis and plant biology, Environ. Pollut. (Barking, Essex: 1987), 157, 42, 10.1016/j.envpol.2008.07.028 Carvalho, 2020, H2O2-retrograde signaling as a pivotal mechanism to understand priming and cross stress tolerance in plants, 57 Choudhury, 2017, Reactive oxygen species, abiotic stress and stress combination, Plant J.: Cell Mol. Biol., 90, 856, 10.1111/tpj.13299 Christmann, 2013, Hydraulic signals in long-distance signaling, Curr. Opin. Plant biol., 16, 293, 10.1016/j.pbi.2013.02.011 Christou, 2022, Safeguarding food security: hormesis-based plant priming to the rescue, Curr. Opin. Environ. Sci. Health, 28 Corpas, 2015, What is the role of hydrogen peroxide in plant peroxisomes?, Plant Biol. (Stuttgart, Germany), 17, 1099, 10.1111/plb.12376 Crawford, 2018, The role of retrograde signals during plant stress responses, J. Exp. Bot., 69, 2783, 10.1093/jxb/erx481 Dat, 1998, Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings, Plant Physiol., 116, 1351, 10.1104/pp.116.4.1351 Dietz, 2021, Synergism and antagonism in plant acclimation to abiotic stress combinations, Turk. J. Bot., 45, 587, 10.3906/bot-2108-45 del Río, 2018, Plant superoxide dismutases: function under abiotic stress conditions, Antioxid. Antioxid. Enzymes Higher Plants, 1 Duarte-Sierra, 2020, Abiotic stress hormesis: an approach to maintain quality, extend storability, and enhance phytochemicals on fresh produce during postharvest, Compreh. Rev. Food Sci. Food saf., 19, 3659, 10.1111/1541-4337.12628 Dunajska-Ordak, 2014, Cloning and expression analysis of a gene encoding for ascorbate peroxidase and responsive to salt stress in beet (Beta vulgaris), Plant Mol. Biol. Rep., 32, 162, 10.1007/s11105-013-0636-6 Ellis, 2014, Beyond allostatic load: rethinking the role of stress in regulating human development, Dev. Psychopathol., 26, 1, 10.1017/S0954579413000849 Erofeeva, 2021, Plant hormesis and shelford's tolerance law curve, J. For. Res., 32, 1789, 10.1007/s11676-021-01312-0 Erofeeva, 2022, Environmental hormesis of non-specific and specific adaptive mechanisms in plants, Sci. Total Environ., 804, 10.1016/j.scitotenv.2021.150059 Erofeeva, 2022, Hormesis in plants: its common occurrence across stresses, Curr. Opin. Toxicol., 30 Fidalgo, 2004, Effects of long-term salt stress on antioxidant defence systems, leaf water relations and chloroplast ultrastructure of potato plants, Ann. Appl. Biol., 145, 185, 10.1111/j.1744-7348.2004.tb00374.x Fink, 2009, Stress: Definition and History, 549 Foyer, 2003, Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria, Physiol. Plant., 119, 355, 10.1034/j.1399-3054.2003.00223.x Foyer, 2005, Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses, Plant Cell, 17, 1866, 10.1105/tpc.105.033589 Foyer, 2013, Redox signaling in plants, Antioxid. Redox Signal., 18, 2087, 10.1089/ars.2013.5278 Gadjev, 2006, Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis, Plant Physiol., 141, 436, 10.1104/pp.106.078717 Gapińska, 2008, Effect of short- and long-term salinity on the activities of antioxidative enzymes and lipid peroxidation in tomato roots, Acta Physiol. Plant., 30, 11, 10.1007/s11738-007-0072-z Goldstein, 2002, Allostasis, homeostats, and the nature of stress, Stress (Amsterdam, Netherlands), 5, 55, 10.1080/102538902900012345 Gratão, 2008, Acquired tolerance of tomato (lycopersicon esculentumcv. micro-tom) plants to cadmium-induced stress, Ann. Appl. Biol., 153, 321, 10.1111/j.1744-7348.2008.00299.x Hadacek, 2010, Hormesis and a chemical raison d'être for secondary plant metabolites, Dose-Resp.: Publ. Int. Hormesis Soc., 9, 79 Hasanuzzaman, 2019, Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress, Antioxidants (Basel, Switzerland), 8, 384 Hertwig, 1992, Light dependence of catalase synthesis and degradation in leaves and the influence of interfering stress conditions, Plant Physiol., 100, 1547, 10.1104/pp.100.3.1547 Hossain, 2015, Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging, Front. Plant Sci., 6, 420, 10.3389/fpls.2015.00420 Hummel, 2010, Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis, Plant Physiol., 154, 357, 10.1104/pp.110.157008 Husak, 2022, Conserved and convergent mechanisms underlying performance-life-history trade-offs, J. Exp. Biol., 225 Inupakutika, 2016, The evolution of reactive oxygen species metabolism, J. Exp. Bot., 67, 5933, 10.1093/jxb/erw382 Iyer, 2008, Enzyme stability and stabilization—aqueous and non-aqueous environment, Process Biochem., 43, 1019, 10.1016/j.procbio.2008.06.004 Jalal, 2021, Hormesis in plants: physiological and biochemical responses, Ecotoxicol. Environ. Saf., 207, 10.1016/j.ecoenv.2020.111225 Jammes, 2009, MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling, Proc. Natl. Acad. Sci., 106, 20520, 10.1073/pnas.0907205106 Jansen, 2017, Stress: the way of life, 254 Jones, 2010, Interdisciplinary approach-advantages, disadvantages, and the future benefits of interdisciplinary studies, Essai, 7, 26 Kamara, 2007, Acclimation of ceratophyllum demersum to stress imposed by phragmites australis and quercus robur leaf extracts, Ecotoxicol. Environ. Saf., 68, 335, 10.1016/j.ecoenv.2007.05.003 Kieffer, 2009, Proteomic and enzymatic response of poplar to cadmium stress, J. Proteom., 72, 379, 10.1016/j.jprot.2009.01.014 Kirillova, 2004, Prikladnaia Biokhimiia I Mikrobiol., 40, 89 Koca, 2007, The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars, Environ. Exp. Bot., 60, 344, 10.1016/j.envexpbot.2006.12.005 Koolhaas, 2011, Stress revisited: a critical evaluation of the stress concept, Neurosci. Biobehav. Rev., 35, 1291, 10.1016/j.neubiorev.2011.02.003 Kupriyanov, 2014, The eustress concept: problems and outlooks, World J. Med. Sci., 11, 179 Laitinen, 2017, A key role for apoplastic H2O2 in Norway spruce phenolic metabolism, Plant Physiol., 174, 1449, 10.1104/pp.17.00085 Larcher, 1980 Lee, 2001, The inductive responses of the antioxidant enzymes by salt stress in the rice (Oryza sativa L.), J. Plant Physiol., 158, 737, 10.1078/0176-1617-00174 Leshem, 2007, Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance, Plant J.: Cell Mol. Biol., 51, 185, 10.1111/j.1365-313X.2007.03134.x Li, 2009, Hormesis, allostatic buffering capacity and physiological mechanism of physical activity: a new theoretic framework, Med. Hypotheses, 72, 527, 10.1016/j.mehy.2008.12.037 Lichtenthaler, 1988, The role of chlorophyll fluorescence in the detection of stress conditions in plants, C R C Crit. Rev. Anal. Chem., 19, 10.1080/15476510.1988.10401466 Liheng, 2009, Pretreatment of seed with H2O2 enhances drought tolerance of wheat (Triticum aestivum L.) seedlings, Afr. J. Biotechnol., 8, 6151, 10.5897/AJB09.490 Liu, 2018, Antagonistic regulation of ABA and GA in metabolism and signaling pathways, Front. Plant Sci., 9, 251, 10.3389/fpls.2018.00251 Mai, 2009, Effect of chilling on photosynthesis and antioxidant enzymes in Hevea brasiliensis Muell. arg, Trees, 23, 863, 10.1007/s00468-009-0328-x Mattson, 2008, Hormesis defined, Ageing Res. Rev., 7, 1, 10.1016/j.arr.2007.08.007 Mattson, 2009, The fundamental role of hormesis in evolution, Hormesis, 57 Mattson, 2010, Hormesis: what it is and why it matters, Hormesis, 1 McCarty, 2016, The alarm phase and the general adaptation syndrome, 13 McEwen, 2004, Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders, Ann. N.Y. Acad. Sci., 1032, 1, 10.1196/annals.1314.001 McEwen, 2003, The concept of allostasis in biology and biomedicine, Hormones Behav., 43, 2, 10.1016/S0018-506X(02)00024-7 Mignolet-Spruyt, 2016, Spreading the news: subcellular and organellar reactive oxygen species production and signalling, J. Exp. Bot., 67, 3831, 10.1093/jxb/erw080 Miller, 2009, The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli, Sci. Signal., 2, ra45, 10.1126/scisignal.2000448 Miller, 2010, Reactive oxygen species homeostasis and signalling during drought and salinity stresses, Plant, Cell Environ., 33, 453, 10.1111/j.1365-3040.2009.02041.x Miller, 2007, Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses, Plant Physiol., 144, 1777, 10.1104/pp.107.101436 Mittler, 2017, ROS are good, Trends Plant Sci., 22, 11, 10.1016/j.tplants.2016.08.002 Mittler, 2004, Reactive oxygen gene network of plants, Trends Plant Sci., 9, 490, 10.1016/j.tplants.2004.08.009 Mittler, 2011, ROS signaling: the new wave?, Trends Plant Sci., 16, 300, 10.1016/j.tplants.2011.03.007 Moller, 2001, Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species, Annu. Rev. Plant Physiol. Plant Mol. Biol., 52, 561, 10.1146/annurev.arplant.52.1.561 Moustakas, 2022, Hormesis in photosystem II: a mechanistic understanding, Curr. Opin. Toxicol., 29, 57, 10.1016/j.cotox.2022.02.003 Mullineaux, 2018, ROS-dependent signalling pathways in plants and algae exposed to high light: comparisons with other eukaryotes, Free Rad. Biol. Med., 122, 52, 10.1016/j.freeradbiomed.2018.01.033 Munck, 1984, Physiological functions of glucocorticoids in stress and their relation to pharmacological actions, Endocrine Rev., 5, 25, 10.1210/edrv-5-1-25 Munns, 2015, Salinity tolerance of crops - what is the cost?, New Phytol., 208, 668, 10.1111/nph.13519 Mushak, 2016, Temporal stability of chemical hormesis (CH): Is CH just a temporary stop on the road to thresholds and toxic responses?, Sci. Total Environ., 569-570, 1446, 10.1016/j.scitotenv.2016.06.233 Niether, 2020, The effect of short-term vs. long-term soil moisture stress on the physiological response of three cocoa (Theobroma cacao L.) cultivars, Plant Growth Regul., 92, 295, 10.1007/s10725-020-00638-9 Noctor, 2016, Intracellular redox compartmentation and ROS-related communication in regulation and signaling, Plant Physiol., 171, 1581, 10.1104/pp.16.00346 Ogasawara, 2008, Synergistic activation of the arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation, J. Biol. Chem., 283, 8885, 10.1074/jbc.M708106200 Pacak, 1998, Heterogeneous neurochemical responses to different stressors: a test of Selye's doctrine of nonspecificity, Am. J. Physiol., 275, R1247 Palma, 2020, Plant catalases as NO and H2S targets, Redox Biol., 34, 10.1016/j.redox.2020.101525 Poschenrieder, 2013, Do toxic ions induce hormesis in plants?, Plant Sci.: Int. J. Exp. Plant Biol., 212, 15, 10.1016/j.plantsci.2013.07.012 Queval, 2011, Increased intracellular H₂O₂ availability preferentially drives glutathione accumulation in vacuoles and chloroplasts, Plant, Cell Environ., 34, 21, 10.1111/j.1365-3040.2010.02222.x Razinger, 2007, Antioxidative responses of duckweed (Lemna minor L.) to short-term copper exposure, Environ. Sci. Pollut. Res. Int., 14, 194, 10.1065/espr2006.11.364 Rodrigues, 2022, Stomata in a state of emergency: H2O2 is the target locked, Trends Plant Sci., 27, 274, 10.1016/j.tplants.2021.10.002 Sako, 2020, Advances in chemical priming to enhance abiotic stress tolerance in plants, Plant Cell Physiol., 61, 1995, 10.1093/pcp/pcaa119 Selye, 1946, The general adaptation syndrome and the diseases of adaptation, J. Clin. Endocrinol. Metab., 6, 117, 10.1210/jcem-6-2-117 Selye, 1964 Sgobba, 2015, Changes in antioxidants are critical in determining cell responses to short- and long-term heat stress, Physiol. Plant., 153, 68, 10.1111/ppl.12220 Shah, 2001, Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings, Plant Sci., 161, 1135, 10.1016/S0168-9452(01)00517-9 Shao, 2007, Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells, Int. J. Biol. Sci., 4, 8 Sharma, 2005, Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings, Plant Growth Regul., 46, 209, 10.1007/s10725-005-0002-2 Sheng, 2014, Superoxide dismutases and superoxide reductases, Chem. Rev., 114, 3854, 10.1021/cr4005296 Shi, 2015, Physiological basis of drought tolerance in potato grown under long-term water deficiency, Int. J. Plant Prod., 9, 305 Sies, 2017, Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: oxidative eustress, Redox Biol., 11, 613, 10.1016/j.redox.2016.12.035 Sies, 2019, Oxidative stress: eustress and distress in redox homeostasis, 153 Smirnoff, 2019, Hydrogen peroxide metabolism and functions in plants, New Phytol., 221, 1197, 10.1111/nph.15488 Soares, 2019, Plants facing oxidative challenges—a little help from the antioxidant networks, Environ. Exp. Bot., 161, 4, 10.1016/j.envexpbot.2018.12.009 Srivastava, 2005, Salinity and copper-induced oxidative damage and changes in the antioxidative defence systems of anabaena doliolum, World J. Microbiol. Biotechnol., 21, 1291, 10.1007/s11274-005-2442-2 Staszek, 2021, ROS metabolism perturbation as an element of mode of action of allelochemicals, Antioxidants (Basel, Switzerland), 10, 1648 Stearns, 1989, Trade-offs in life-history evolution, Funct. Ecol., 3, 259, 10.2307/2389364 Sterling, 1988, Allostasis: a new paradigm to explain arousal pathology, 629 Straus, 2010, Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in arabidopsis, Plant J.: Cell Mol. Biol., 62, 628, 10.1111/j.1365-313X.2010.04178.x Strobel, 1995, Chemical and biological inducers of systemic resistance to pathogens protect cucumber and tobacco plants from damage caused by paraquat and cupric chloride, Phytopathology, 85, 1306, 10.1094/Phyto-85-1306 Sun, 2015, Proline, sugars, and antioxidant enzymes respond to drought stress in the leaves of Strawberry Plants, Korean J. Hortic. Sci. Technol., 33, 625, 10.7235/hort.2015.15054 Suzuki, 2011, Respiratory burst oxidases: the engines of ROS signaling, Curr. Opin. Plant Biol., 14, 691, 10.1016/j.pbi.2011.07.014 Suzuki, 2013, Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants, Plant Cell, 25, 3553, 10.1105/tpc.113.114595 Takeda, 2008, Local positive feedback regulation determines cell shape in root hair cells, Science, 319, 1241, 10.1126/science.1152505 Uzilday, 2012, Comparison of ROS formation and antioxidant enzymes in Cleome gynandra (C₄) and Cleome spinosa (C₃) under drought stress, Plant Sci.: Int. J. Exp. Plant Biol., 182, 59, 10.1016/j.plantsci.2011.03.015 Veljović Jovanović, 2018, Class III peroxidases: functions, localization and redox regulation of isoenzymes, Antioxid. Antioxid. Enzymes Higher Plants, 269, 10.1007/978-3-319-75088-0_13 Voothuluru, 2020, Apoplastic hydrogen peroxide in the growth zone of the maize primary root. increased levels differentially modulate root elongation under well-watered and water-stressed conditions, Front. Plant Sci., 11, 392, 10.3389/fpls.2020.00392 Wagner, 2011, Approaches to understanding and measuring interdisciplinary scientific research (IDR): a review of the literature, J. Inform., 5, 14, 10.1016/j.joi.2010.06.004 Wang, 2014, Free radicals mediate systemic acquired resistance, Cell Rep., 7, 348, 10.1016/j.celrep.2014.03.032 Wang, 2013, Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple, J. Pineal Res., 54, 292, 10.1111/jpi.12017 Wei, 2022, Hormetic effects of zinc on growth and antioxidant defense system of wheat plants, Sci. Total Environ., 807, 10.1016/j.scitotenv.2021.150992 Wingfield, 2003, Control of behavioural strategies for capricious environments, Anim. Behav., 66, 807, 10.1006/anbe.2003.2298 Yang, 2009, Chitosan enhances leaf membrane stability and antioxidant enzyme activities in apple seedlings under drought stress, Plant Growth Regul., 58, 131, 10.1007/s10725-009-9361-4 Yang, 2015, Stress sensitivity is associated with differential accumulation of reactive oxygen and nitrogen species in maize genotypes with contrasting levels of drought tolerance, Int. J. Mol. Sci., 16, 24791, 10.3390/ijms161024791 Zhang, 2001, Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba, Plant Physiol., 126, 1438, 10.1104/pp.126.4.1438 Zheng, 2021, The proline cycle as an eukaryotic redox valve, J. Exp. Bot., 72, 6856, 10.1093/jxb/erab361