Signaling Toward Reactive Oxygen Species-Scavenging Enzymes in Plants
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection
Document type Journal Article, Review
PubMed
33597960
PubMed Central
PMC7882706
DOI
10.3389/fpls.2020.618835
Knihovny.cz E-resources
- Keywords
- antioxidant enzymes, calcium, mitogen-activated protein kinases, oxidative stress, plants, reactive oxygen species, signaling, stress,
- Publication type
- Journal Article MeSH
- Review MeSH
Reactive oxygen species (ROS) are signaling molecules essential for plant responses to abiotic and biotic stimuli as well as for multiple developmental processes. They are produced as byproducts of aerobic metabolism and are affected by adverse environmental conditions. The ROS content is controlled on the side of their production but also by scavenging machinery. Antioxidant enzymes represent a major ROS-scavenging force and are crucial for stress tolerance in plants. Enzymatic antioxidant defense occurs as a series of redox reactions for ROS elimination. Therefore, the deregulation of the antioxidant machinery may lead to the overaccumulation of ROS in plants, with negative consequences both in terms of plant development and resistance to environmental challenges. The transcriptional activation of antioxidant enzymes accompanies the long-term exposure of plants to unfavorable environmental conditions. Fast ROS production requires the immediate mobilization of the antioxidant defense system, which may occur via retrograde signaling, redox-based modifications, and the phosphorylation of ROS detoxifying enzymes. This review aimed to summarize the current knowledge on signaling processes regulating the enzymatic antioxidant capacity of plants.
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Adachi H., Nakano T., Miyagawa N., Ishihama N., Yoshioka M., Katou Y., et al. . (2015). WRKY transcription factors phosphorylated by MAPK regulate a plant immune NADPH oxidase in Nicotiana benthamiana. Plant Cell 27, 2645–2663. 10.1105/tpc.15.00213 PubMed DOI PMC
Ahmad A., Khan W. U., Shah A. A., Yasin N. A., Naz S., Ali A., et al. . (2020). Synergistic effects of nitric oxide and silicon on promoting plant growth, oxidative stress tolerance and reduction of arsenic uptake in Brassica juncea. Chemosphere 262:128384. 10.1016/j.chemosphere.2020.128384 PubMed DOI
Alscher R. G., Erturk N., Heath L. S. (2002). Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J. Exp. Bot. 53, 1331–1341. 10.1093/jexbot/53.372.1331 PubMed DOI
Apel K., Hirt H. (2004). REACTIVE OXYGEN SPECIES: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399. 10.1146/annurev.arplant.55.031903.141701 PubMed DOI
Araki R., Mermod M., Yamasaki H., Kamiya T., Fujiwara T., Shikanai T. (2018). SPL7 locally regulates copper-homeostasis-related genes in Arabidopsis. J. Plant Physiol. 224–225, 137–143. 10.1016/j.jplph.2018.03.014 PubMed DOI
Arsova B., Watt M., Usadel B. (2018). Monitoring of plant protein post-translational modifications using targeted proteomics. Front. Plant Sci. 9:1168. 10.3389/fpls.2018.01168 PubMed DOI PMC
Asano T., Hayashi N., Kobayashi M., Aoki N., Miyao A., Mitsuhara I., et al. . (2012). A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant J. 69, 26–36. 10.1111/j.1365-313X.2011.04766.x PubMed DOI
Atif R. M., Shahid L., Waqas M., Ali B., Rashid M. A. R., Azeem F., et al. . (2019). Insights on calcium-dependent protein kinases (CPKs) signaling for abiotic stress tolerance in plants. Int. J. Mol. Sci. 20:5298. 10.3390/ijms20215298 PubMed DOI PMC
Baxter A., Mittler R., Suzuki N. (2014). ROS as key players in plant stress signalling. J. Exp. Bot. 65, 1229–1240. 10.1093/jxb/ert375 PubMed DOI
Begara-Morales J. C., Sánchez-Calvo B., Chaki M., Mata-Pérez C., Valderrama R., Padilla M. N., et al. . (2015). Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J. Exp. Bot. 66, 5983–5996. 10.1093/jxb/erv306 PubMed DOI PMC
Begara-Morales J. C., Sánchez-Calvo B., Chaki M., Valderrama R., Mata-Pérez C., López-Jaramillo J., et al. . (2014). Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J. Exp. Bot. 65, 527–538. 10.1093/jxb/ert396 PubMed DOI PMC
Berkholz D. S., Faber H. R., Savvides S. N., Karplus P. A. (2008). Catalytic cycle of human glutathione reductase near 1 A resolution. J. Mol. Biol. 382, 371–384. 10.1016/j.jmb.2008.06.083 PubMed DOI PMC
Bethke G., Unthan T., Uhrig J. F., Pöschl Y., Gust A. A., Scheel D., et al. . (2009). Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc. Natl. Acad. Sci. U.S.A. 106, 8067–8072. 10.1073/pnas.0810206106 PubMed DOI PMC
Bhaskara G. B., Wen T. N., Nguyen T. T., Verslues P. E. (2017). Protein phosphatase 2Cs and Microtubule-Associated Stress Protein 1 control microtubule stability, plant growth, and drought response. Plant Cell 29, 169–191. 10.1105/tpc.16.00847 PubMed DOI PMC
Bindschedler L. V., Dewdney J., Blee K. A., Stone J. M., Asai T., Plotnikov J., et al. . (2006). Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J. 47, 851–863. 10.1111/j.1365-313X.2006.02837.x PubMed DOI PMC
Boudsocq M., Willmann M. R., McCormack M., Lee H., Shan L., He P., et al. . (2010). Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464, 418–422. 10.1038/nature08794 PubMed DOI PMC
Bueso E., Alejandro S., Carbonell P., Perez-Amador M. A., Fayos J., Bellés J. M., et al. . (2007). The lithium tolerance of the Arabidopsis cat2 mutant reveals a cross-talk between oxidative stress and ethylene. Plant J. 52, 1052–1065. 10.1111/j.1365-313X.2007.03305.x PubMed DOI
Bykova N. V., Egsgaard H., Møller I. M. (2003). Identification of 14 new phosphoproteins involved in important plant mitochondrial processes. FEBS Lett. 540, 141–146. 10.1016/s0014-5793(03)00250-3 PubMed DOI
Candas D., Fan M., Nantajit D., Vaughan A. T., Murley J. S., Woloschak, et al. . (2013). CyclinB1/Cdk1 phosphorylates mitochondrial antioxidant MnSOD in cell adaptive response to radiation stress. J. Mol. Cell Biol. 5, 166–175. 10.1093/jmcb/mjs062 PubMed DOI PMC
Chaki M., Álvarez de Morales P., Ruiz C., Begara-Morales J. C., Barroso J. B., Corpas F. J., et al. . (2015). Ripening of pepper (Capsicum annuum) fruit is characterized by an enhancement of protein tyrosine nitration. Ann. Bot. 116, 637–647. 10.1093/aob/mcv016 PubMed DOI PMC
Chan K. X., Phua S. Y., Crisp P., McQuinn R., Pogson B. J. (2016). Learning the languages of the chloroplast: retrograde signaling and beyond. Annu. Rev. Plant Biol. 67, 25–53. 10.1146/annurev-arplant-043015-111854 PubMed DOI
Chang R., Jang C. J., Branco-Price C., Nghiem P., Bailey-Serres J. (2012). Transient MPK6 activation in response to oxygen deprivation and reoxygenation is mediated by mitochondria and aids seedling survival in Arabidopsis. Plant Mol. Biol. 78, 109–122. 10.1007/s11103-011-9850-5 PubMed DOI
Chen C., Letnik I., Hacham Y., Dobrev P., Ben-Daniel B. H., Vanková R., et al. . (2014). ASCORBATE PEROXIDASE6 protects Arabidopsis desiccating and germinating seeds from stress and mediates cross talk between reactive oxygen species, abscisic acid, and auxin. Plant Physiol. 166, 370–383. 10.1104/pp.114.245324 PubMed DOI PMC
Chen L., Wu R., Feng J., Feng T., Wang C., Hu J., et al. . (2020). Transnitrosylation mediated by the non-canonical catalase ROG1 regulates nitric oxide signaling in plants. Dev. Cell 53, 444–457.e5. 10.1016/j.devcel.2020.03.020 PubMed DOI
Chew O., Whelan J., Millar A. H. (2003). Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J. Biol. Chem. 278, 46869–46877. 10.1074/jbc.M307525200 PubMed DOI
Chin D. C., Senthil Kumar R., Suen C. S., Chien C. Y., Hwang M. J., Hsu C. H., et al. . (2019). Plant cytosolic ascorbate peroxidase with dual catalytic activity modulates abiotic stress tolerances. iScience 16, 31–49. 10.1016/j.isci.2019.05.014 PubMed DOI PMC
Chmielowska-Bak J., Gzyl J., Rucińska-Sobkowiak R., Arasimowicz-Jelonek M., Deckert J. (2014). The new insights into cadmium sensing. Front. Plant Sci. 5:245. 10.3389/fpls.2014.00245 PubMed DOI PMC
Choi W. G., Toyota M., Kim S. H., Hilleary R., Gilroy S. (2014). Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc. Natl. Acad. Sci. U.S.A. 111, 6497–6502. 10.1073/pnas.1319955111 PubMed DOI PMC
Choudhary M. K., Nomura Y., Wang L., Nakagami H., Somers D. E. (2015). Quantitative circadian phosphoproteomic analysis of Arabidopsis reveals extensive clock control of key components in physiological, metabolic, and signaling pathways. Mol. Cell Proteomics 14, 2243–2260. 10.1074/mcp.M114.047183 PubMed DOI PMC
Ciacka K., Tymiński M., Gniazdowska A., Krasuska U. (2020). Carbonylation of proteins-an element of plant ageing. Planta 252:12. 10.1007/s00425-020-03414-1 PubMed DOI PMC
Cohu C. M., Abdel-Ghany S. E., Gogolin Reynolds K. A., Onofrio A. M., Bodecker J. R., Kimbrel J. A., et al. . (2009). Copper delivery by the copper chaperone for chloroplast and cytosolic copper/zinc-superoxide dismutases: regulation and unexpected phenotypes in an Arabidopsis mutant. Mol. Plant. 2, 1336–1350. 10.1093/mp/ssp084 PubMed DOI
Colcombet J., Hirt H. (2008). Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem. J. 413, 217–226. 10.1042/BJ20080625 PubMed DOI
Considine M. J., Foyer C. H. (2014). Redox regulation of plant development. Antioxid. Redox Signal. 21, 1305–1326. 10.1089/ars.2013.5665 PubMed DOI PMC
Corcoran A., Cotter T. G. (2013). Redox regulation of protein kinases. FEBS J. 280, 1944–1965. 10.1111/febs.12224 PubMed DOI
Corpas F. J., Barroso J. B. (2017). Lead-induced stress, which triggers the production of nitric oxide (NO) and superoxide anion (O2·−) in Arabidopsis peroxisomes, affects catalase activity. Nitric Oxide 68, 103–110. 10.1016/j.niox.2016.12.010 PubMed DOI
Csiszár J., Brunner S., Horváth E., Bela K., Ködmön P., Riyazuddin R., et al. (2018). Exogenously applied salicylic acid maintains redox homeostasis in salt-stressed Arabidopsis gr1 mutants expressing cytosolic roGFP1. Plant Growth Regul. 86, 181–194. 10.1007/s10725-018-0420-6 DOI
Cui F., Brosché M., Shapiguzov A., He X. Q., Vainonen J. P., Leppälä J., et al. . (2019). Interaction of methyl viologen-induced chloroplast and mitochondrial signalling in Arabidopsis. Free Radic. Biol. Med. 134, 555–566. 10.1016/j.freeradbiomed.2019.02.006 PubMed DOI
Cui J., Jiang N., Zhou X., Hou X., Yang G., Meng J., et al. . (2018). Tomato MYB49 enhances resistance to Phytophthora infestans and tolerance to water deficit and salt stress. Planta 248, 1487–1503. 10.1007/s00425-018-2987-6 PubMed DOI
Dalle-Donne I., Rossi R., Giustarini D., Milzani A., Colombo R. (2003). Protein carbonyl groups as biomarkers of oxidative stress. Clin. Chim. Acta 329, 23–38. 10.1016/s0009-8981(03)00003-2 PubMed DOI
Danquah A., de Zelicourt A., Colcombet J., Hirt H. (2014). The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol. Adv. 32, 40–52. 10.1016/j.biotechadv.2013.09.006 PubMed DOI
Davletova S., Rizhsky L., Liang H., Shengqiang Z., Oliver D. J., Coutu J., et al. . (2005a). Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17, 268–281. 10.1105/tpc.104.026971 PubMed DOI PMC
Davletova S., Schlauch K., Coutu J., Mittler R. (2005b). The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol. 139, 847–856. 10.1104/pp.105.068254 PubMed DOI PMC
De Pinto M. C., Locato V., De Gara L. (2012). Redox regulation in plant programmed cell death: redox regulation in plant PCD. Plant Cell Environ. 35, 234–244. 10.1111/j.1365-3040.2011.02387.x PubMed DOI
del Río L. A. (2015). ROS and RNS in plant physiology: an overview. J. Exp. Bot. 66, 2827–2837. 10.1093/jxb/erv099 PubMed DOI
del Río L. A., López-Huertas E. (2016). ROS Generation in peroxisomes and its role in cell signaling. Plant Cell Physiol. 57, 1364–1376. 10.1093/pcp/pcw076 PubMed DOI
del Río L. A., Sandalio L. M., Corpas F. J., Palma J. M., Barroso J. B. (2006). Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol. 141, 330–335. 10.1104/pp.106.078204 PubMed DOI PMC
Delledonne M., Zeier J., Marocco A., Lamb C. (2001). Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl. Acad. Sci. U.S.A. 98, 13454–13459. 10.1073/pnas.231178298 PubMed DOI PMC
Demidchik V. (2018). ROS-Activated ion channels in plants: biophysical characteristics, physiological functions and molecular nature. Int. J. Mol. Sci. 19, 1263. 10.3390/ijms19041263 PubMed DOI PMC
Demidchik V., Shabala S., Isayenkov S., Cuin T. A., Pottosin I. (2018). Calcium transport across plant membranes: mechanisms and functions. New Phytol. 220, 49–69. 10.1111/nph.15266 PubMed DOI
Diao Y., Liu W., Wong C. C. L., Wang X., Lee K., Cheung P.-Y., et al. . (2010). Oxidation-induced intramolecular disulfide bond inactivates mitogen-activated protein kinase 6 by inhibiting ATP binding. Proc. Natl. Acad. Sci. U.S.A. 107, 20974–20979. 10.1073/pnas.1007225107 PubMed DOI PMC
Dietz K.-J. (2011). Peroxiredoxins in plants and cyanobacteria. Antioxid. Redox Signal. 15, 1129–1159. 10.1089/ars.2010.3657 PubMed DOI PMC
Dietz K.-J. (2014). Redox regulation of transcription factors in plant stress acclimation and development. Antioxid. Redox Signal. 21, 1356–1372. 10.1089/ars.2013.5672 PubMed DOI
Ding H., Wang B., Han Y., Li S. (2020). The pivotal function of dehydroascorbate reductase in glutathione homeostasis in plants. J. Exp. Bot. 71, 3405–3416. 10.1093/jxb/eraa107 PubMed DOI
Dóczi R., Brader G., Pettkó-Szandtner A., Rajh I., Djamei A., Pitzschke A., et al. . (2007). The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell 19, 3266–3279. 10.1105/tpc.106.050039 PubMed DOI PMC
Dodd A. N., Kudla J., Sanders D. (2010). The language of calcium signaling. Annu. Rev. Plant Biol. 61, 593–620. 10.1146/annurev-arplant-070109-104628 PubMed DOI
Doll J., Muth M., Riester L., Nebel S., Bresson J., Lee H. C., et al. . (2020). Arabidopsis thaliana WRKY25 transcription factor mediates oxidative stress tolerance and regulates senescence in a redox-dependent manner. Front. Plant Sci. 10:1734. 10.3389/fpls.2019.01734 PubMed DOI PMC
Du Y. Y., Wang P. C., Chen J., Song C. P. (2008). Comprehensive functional analysis of the catalase gene family in Arabidopsis thaliana. J. Integr. Plant Biol. 50, 1318–1326. 10.1111/j.1744-7909.2008.00741.x PubMed DOI
Dubiella U., Seybold H., Durian G., Komander E., Lassig R., Witte C.-P., et al. . (2013). Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc. Natl. Acad. Sci. U.S.A. 110, 8744–8749. 10.1073/pnas.1221294110 PubMed DOI PMC
Dugas D. V., Bartel B. (2008). Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol. Biol. 67, 403–417. 10.1007/s11103-008-9329-1 PubMed DOI
Dvořák P., Krasylenko Y., Ovečka M., Basheer J., Zapletalová V., Šamaj J., et al. . (2020). In-vivo light-sheet microscopy resolves localisation patterns of FSD1, a superoxide dismutase with function in root development and osmoprotection. Plant Cell Environ. 44, 68–87. 10.1111/pce.13894 PubMed DOI
Eastmond P. J. (2007). MONODEHYROASCORBATE REDUCTASE4 is required for seed storage oil hydrolysis and postgerminative growth in Arabidopsis. Plant Cell 19, 1376–1387. 10.1105/tpc.106.043992 PubMed DOI PMC
Eltayeb A. E., Kawano N., Badawi G. H., Kaminaka H., Sanekata T., Shibahara T., et al. . (2007). Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta 225, 1255–1264. 10.1007/s00425-006-0417-7 PubMed DOI
Eltayeb A. E., Yamamoto S., Habora M. E. E., Yin L., Tsujimoto H., Tanaka K. (2011). Transgenic potato overexpressing Arabidopsis cytosolic AtDHAR1 showed higher tolerance to herbicide, drought and salt stresses. Breed. Sci. 61, 3–10. 10.1270/jsbbs.61.3 DOI
Engelsberger W. R., Schulze W. X. (2012). Nitrate and ammonium lead to distinct global dynamic phosphorylation patterns when resupplied to nitrogen-starved Arabidopsis seedlings. Plant J. 69, 978–995. 10.1111/j.1365-313X.2011.04848.x PubMed DOI PMC
Eubel H., Meyer E. H., Taylor N. L., Bussell J. D., O'Toole N., Heazlewood J. L., et al. . (2008). Novel proteins, putative membrane transporters, and an integrated metabolic network are revealed by quantitative proteomic analysis of Arabidopsis cell culture peroxisomes. Plant Physiol. 148, 1809–1829. 10.1104/pp.108.129999 PubMed DOI PMC
Exposito-Rodriguez M., Laissue P. P., Yvon-Durocher G., Smirnoff N., Mullineaux P. M. (2017). Photosynthesis-dependent H2O2 transfer from chloroplasts to nuclei provides a high-light signalling mechanism. Nat. Commun. 8:49. 10.1038/s41467-017-00074-w PubMed DOI PMC
Farnese F. S., Menezes-Silva P. E., Gusman G. S., Oliveira J. A. (2016). When bad guys become good ones: the key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress. Front. Plant Sci. 7:471. 10.3389/fpls.2016.00471 PubMed DOI PMC
Fay J. M., Zhu C., Proctor E. A., Tao Y., Cui W., Ke H., et al. . (2016). A phosphomimetic mutation stabilizes SOD1 and rescues cell viability in the context of an ALS-associated mutation. Structure 24, 1898–1906. 10.1016/j.str.2016.08.011 PubMed DOI PMC
Feng H., Wang X., Zhang Q., Fu Y., Feng C., Wang B., et al. . (2014). Monodehydroascorbate reductase gene, regulated by the wheat PN-2013 miRNA, contributes to adult wheat plant resistance to stripe rust through ROS metabolism. Biochim. Biophys. Acta 1839, 1–12. 10.1016/j.bbagrm.2013.11.001 PubMed DOI
Foyer C. H. (2018). Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. Environ. Exp. Bot. 154, 134–142. 10.1016/j.envexpbot.2018.05.003 PubMed DOI PMC
Foyer C. H., Noctor G. (2011). Ascorbate and glutathione: the heart of the redox hub. Plant Physiol. 155, 2–18. 10.1104/pp.110.167569 PubMed DOI PMC
Foyer C. H., Noctor G. (2020). Redox homeostasis and signaling in a higher-CO2 world. Annu. Rev. Plant Biol. 71, 157–182. 10.1146/annurev-arplant-050718-095955 PubMed DOI
Frugoli J. A., Zhong H. H., Nuccio M. L., McCourt P., McPeek M. A., Thomas T. L., et al. . (1996). Catalase is encoded by a multigene family in Arabidopsis thaliana (L.) Heynh. Plant Physiol. 112, 327–336. 10.1104/pp.112.1.327 PubMed DOI PMC
Gadjev I., Vanderauwera S., Gechev T. S., Laloi C., Minkov I. N., Shulaev V., et al. . (2006). Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141, 436–445. 10.1104/pp.106.078717 PubMed DOI PMC
Gallie D. R., Chen Z. (2019). Chloroplast-localized iron superoxide dismutases FSD2 and FSD3 are functionally distinct in Arabidopsis. PLoS ONE 14:e0220078. 10.1371/journal.pone.0220078 PubMed DOI PMC
Garcia-Molina A., Xing S., Huijser P. (2014). Functional characterisation of Arabidopsis SPL7 conserved protein domains suggests novel regulatory mechanisms in the Cu deficiency response. BMC Plant Biol. 14:231. 10.1186/s12870-014-0231-5 PubMed DOI PMC
Gaupels F., Durner J., Kogel K.-H. (2017). Production, amplification and systemic propagation of redox messengers in plants? The phloem can do it all! New Phytol. 214, 554–560. 10.1111/nph.14399 PubMed DOI
Gawroński P., Witoń D., Vashutina K., Bederska M., Betliński B., Rusaczonek A., et al. . (2014). Mitogen-activated protein kinase 4 is a salicylic acid-independent regulator of growth but not of photosynthesis in Arabidopsis. Mol. Plant. 7, 1151–1166. 10.1093/mp/ssu060 PubMed DOI
Geilfus C.-M., Niehaus K., Gödde V., Hasler M., Zörb C., Gorzolka K., et al. . (2015). Fast responses of metabolites in Vicia faba L. to moderate NaCl stress. Plant Physiol. Biochem. 92, 19–29. 10.1016/j.plaphy.2015.04.008 PubMed DOI
Gilroy S., Białasek M., Suzuki N., Górecka M., Devireddy A. R., Karpiński S., et al. . (2016). ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol. 171, 1606–1615. 10.1104/pp.16.00434 PubMed DOI PMC
Gilroy S., Suzuki N., Miller G., Choi W.-G., Toyota M., Devireddy A. R., et al. . (2014). A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci. 19, 623–630. 10.1016/j.tplants.2014.06.013 PubMed DOI
Gleason C., Huang S., Thatcher L. F., Foley R. C., Anderson C. R., Carroll A. J., et al. . (2011). Mitochondrial complex II has a key role in mitochondrial-derived reactive oxygen species influence on plant stress gene regulation and defense. Proc. Natl. Acad. Sci. U.S.A. 108, 10768–10773. 10.1073/pnas.1016060108 PubMed DOI PMC
Gou J. Y., Li K., Wu K., Wang X., Lin H., Cantu D., et al. . (2015). Wheat stripe rust resistance protein WKS1 reduces the ability of the thylakoid-associated ascorbate peroxidase to detoxify reactive oxygen species. Plant Cell 27, 1755–1770. 10.1105/tpc.114.134296 PubMed DOI PMC
Granlund I., Storm P., Schubert M., García-Cerdán J. G., Funk C., Schröder W. P. (2009). The TL29 protein is lumen located, associated with PSII and not an ascorbate peroxidase. Plant Cell Physiol. 50, 1898–1910. 10.1093/pcp/pcp134 PubMed DOI
Gudesblat G. E., Iusem N. D., Morris P. C. (2007). Guard cell-specific inhibition of Arabidopsis MPK3 expression causes abnormal stomatal responses to abscisic acid and hydrogen peroxide. New Phytol. 173, 713–721. 10.1111/j.1469-8137.2006.01953.x PubMed DOI
Guo B., Liu C., Li H., Yi K., Ding N., Li N., et al. . (2016). Endogenous salicylic acid is required for promoting cadmium tolerance of Arabidopsis by modulating glutathione metabolisms. J. Hazard. Mater. 316, 77–86. 10.1016/j.jhazmat.2016.05.032 PubMed DOI
Guo P., Li Z., Huang P., Li B., Fang S., Chu J., et al. . (2017). A tripartite amplification loop involving the transcription factor WRKY75, salicylic acid, and reactive oxygen species accelerates leaf senescence. Plant Cell 29, 2854–2870. 10.1105/tpc.17.00438 PubMed DOI PMC
Hackenberg T., Juul T., Auzina A., Gwizdz S., Malolepszy A., Van Der Kelen K., et al. . (2013). Catalase and NO CATALASE ACTIVITY1 promote autophagy-dependent cell death in Arabidopsis. Plant Cell 25, 4616–4626. 10.1105/tpc.113.117192 PubMed DOI PMC
He H., Van Breusegem F., Mhamdi A. (2018). Redox-dependent control of nuclear transcription in plants. J. Exp. Bot. 69, 3359–3372. 10.1093/jxb/ery130 PubMed DOI
He J., Ren Y., Chen X., Chen H. (2014). Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa L.) under cadmium stress. Ecotoxicol. Environ. Saf. 108, 114–119. 10.1016/j.ecoenv.2014.05.021 PubMed DOI
Hehl R., Norval L., Romanov A., Bülow L. (2016). Boosting AthaMap database content with data from protein binding microarrays. Plant Cell Physiol. 57:e4. 10.1093/pcp/pcv156 PubMed DOI
Hiltscher H., Rudnik R., Shaikhali J., Heiber I., Mellenthin M., Duarte I. M., et al. . (2014). The radical induced cell death protein 1 (RCD1) supports transcriptional activation of genes for chloroplast antioxidant enzymes. Front. Plant Sci. 5:475. 10.3389/fpls.2014.00475 PubMed DOI PMC
Holzmeister C., Gaupels F., Geerlof A., Sarioglu H., Sattler M., Durner J., et al. . (2015). Differential inhibition of Arabidopsis superoxide dismutases by peroxynitrite-mediated tyrosine nitration. J. Exp. Bot. 66, 989–999. 10.1093/jxb/eru458 PubMed DOI PMC
Horváth E., Szalai G., Janda T. (2007). Induction of abiotic stress tolerance by salicylic acid signaling. J. Plant Growth Regul. 26, 290–300. 10.1007/s00344-007-9017-4 DOI
Hu C.-H., Wang P.-Q., Zhang P.-P., Nie X.-M., Li B.-B., Tai L., et al. . (2020). NADPH Oxidases: the vital performers and center hubs during plant growth and signaling. Cells 9:437. 10.3390/cells9020437 PubMed DOI PMC
Huang L., Jia J., Zhao X., Zhang M., Huang X., Ji E., et al. . (2018). The ascorbate peroxidase APX1 is a direct target of a zinc finger transcription factor ZFP36 and a late embryogenesis abundant protein OsLEA5 interacts with ZFP36 to co-regulate OsAPX1 in seed germination in rice. Biochem. Biophys. Res. Commun. 495, 339–345. 10.1016/j.bbrc.2017.10.128 PubMed DOI
Huang W., Yang Y.-J., Zhang S.-B. (2019). The role of water-water cycle in regulating the redox state of photosystem I under fluctuating light. Biochim. Biophys. Acta 1860, 383–390. 10.1016/j.bbabio.2019.03.007 PubMed DOI
Huda K. M. K., Banu M. S. A., Garg B., Tula S., Tuteja R., Tuteja N. (2013). OsACA6, a P-type IIB Ca2+ATPase promotes salinity and drought stress tolerance in tobacco by ROS scavenging and enhancing the expression of stress-responsive genes. Plant J. 76, 997–1015. 10.1111/tpj.12352 PubMed DOI
Hwang J. E., Lim C. J., Chen H., Je J., Song C., Lim C. O. (2012). Overexpression of Arabidopsis dehydration- responsive element-binding protein 2C confers tolerance to oxidative stress. Mol. Cells 33, 135–140. 10.1007/s10059-012-2188-2 PubMed DOI PMC
Innocenti G., Pucciariello C., Le Gleuher M., Hopkins J., de Stefano M., Delledonne M., et al. . (2007). Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225, 1597–1602. 10.1007/s00425-006-0461-3 PubMed DOI
Jammes F., Song C., Shin D., Munemasa S., Takeda K., Gu D., et al. . (2009). MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. Proc. Natl. Acad. Sci. U.S.A. 106, 20520–20525. 10.1073/pnas.0907205106 PubMed DOI PMC
Jin C., Qin L., Shi Y., Candas D., Fan M., Lu C. L., et al. . (2015). CDK4-mediated MnSOD activation and mitochondrial homeostasis in radioadaptive protection. Free Radic. Biol. Med. 81, 77–87. 10.1016/j.freeradbiomed.2014.12.026 PubMed DOI PMC
Joo J. H., Bae Y. S., Lee J. S. (2001). Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol. 126, 1055–1060. 10.1104/pp.126.3.1055 PubMed DOI PMC
Jung H. S., Crisp P. A., Estavillo G. M., Cole B., Hong F., Mockler T. C., et al. . (2013). Subset of heat-shock transcription factors required for the early response of Arabidopsis to excess light. Proc. Natl. Acad. Sci. U.S.A. 110, 14474–14479. 10.1073/pnas.1311632110 PubMed DOI PMC
Kang Z., Qin T., Zhao Z. (2019). Thioredoxins and thioredoxin reductase in chloroplasts: a review. Gene 706, 32–42. 10.1016/j.gene.2019.04.041 PubMed DOI
Kangasjärvi S., Lepistö A., Hännikäinen K., Piippo M., Luomala E. M., Aro E. M., et al. . (2008). Diverse roles for chloroplast stromal and thylakoid-bound ascorbate peroxidases in plant stress responses. Biochem. J. 412, 275–285. 10.1042/BJ20080030 PubMed DOI
Karpinski S., Escobar C., Karpinska B., Creissen G., Mullineaux P. M. (1997). Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9, 627–640. 10.1105/tpc.9.4.627 PubMed DOI PMC
Kataya A. R., Reumann S. (2010). Arabidopsis glutathione reductase 1 is dually targeted to peroxisomes and the cytosol. Plant Signal. Behav. 5, 171–175. 10.4161/psb.5.2.10527 PubMed DOI PMC
Kaur N., Hu J. (2011). Defining the plant peroxisomal proteome: from Arabidopsis to rice. Front. Plant Sci. 2:103. 10.3389/fpls.2011.00103 PubMed DOI PMC
Khan M. I., Fatma M., Per T. S., Anjum N. A., Khan N. A. (2015). Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front. Plant Sci. 6:462. 10.3389/fpls.2015.00462 PubMed DOI PMC
Khedia J., Agarwal P., Agarwal P. K. (2019). Deciphering hydrogen peroxide-induced signalling towards stress tolerance in plants. 3 Biotech 9, 395. 10.1007/s13205-019-1924-0 PubMed DOI PMC
Khraiwesh B., Zhu J. K., Zhu J. (2012). Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim. Biophys. Acta 1819, 137–148. 10.1016/j.bbagrm.2011.05.001 PubMed DOI PMC
Klein P., Seidel T., Stöcker B., Dietz K. J. (2012). The membrane-tethered transcription factor ANAC089 serves as redox-dependent suppressor of stromal ascorbate peroxidase gene expression. Front. Plant Sci. 3:247. 10.3389/fpls.2012.00247 PubMed DOI PMC
Kliebenstein D. J., Monde R. A., Last R. L. (1998). Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol. 118, 637–650. 10.1104/pp.118.2.637 PubMed DOI PMC
Kneeshaw S., Keyani R., Delorme-Hinoux V., Imrie L., Loake G. J., Le Bihan T., et al. . (2017). Nucleoredoxin guards against oxidative stress by protecting antioxidant enzymes. Proc. Natl. Acad. Sci. U.S.A. 114, 8414–8419. 10.1073/pnas.1703344114 PubMed DOI PMC
Kobayashi M., Ohura I., Kawakita K., Yokota N., Fujiwara M., Shimamoto K., et al. . (2007). Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19, 1065–1080. 10.1105/tpc.106.048884 PubMed DOI PMC
Kohli S. K., Khanna K., Bhardwaj R., Abd Allah E. F., Ahmad P., Corpas F. J. (2019). Assessment of subcellular ROS and NO metabolism in higher plants: multifunctional signaling molecules. Antioxidants 8:641. 10.3390/antiox8120641 PubMed DOI PMC
Komis G., Šamajová O., Ovečka M., Šamaj J. (2018). Cell and developmental biology of plant mitogen-activated protein kinases. Annu. Rev. Plant Biol. 69, 237–265. 10.1146/annurev-arplant-042817-040314 PubMed DOI
Kornyeyev D., Logan B. A., Payton P. R., Allen R. D., Holaday A. S. (2003). Elevated chloroplastic glutathione reductase activities decrease chilling-induced photoinhibition by increasing rates of photochemistry, but not thermal energy dissipation, in transgenic cotton. Funct. Plant Biol. 30, 101–110. 10.1071/FP02144 PubMed DOI
Koussevitzky S., Suzuki N., Huntington S., Armijo L., Sha W., Cortes D., et al. . (2008). Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J. Biol. Chem. 283, 34197–34203. 10.1074/jbc.M806337200 PubMed DOI PMC
Kovacs I., Holzmeister C., Wirtz M., Geerlof A., Fröhlich T., Römling G., et al. . (2016). ROS-mediated inhibition of S-nitrosoglutathione reductase contributes to the activation of anti-oxidative Mechanisms. Front. Plant Sci. 7:1669. 10.3389/fpls.2016.01669 PubMed DOI PMC
Kovtun Y., Chiu W. L., Tena G., Sheen J. (2000). Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. U.S.A. 97, 2940–2945. 10.1073/pnas.97.6.2940 PubMed DOI PMC
Kreps J. A., Wu Y., Chang H. S., Zhu T., Wang X., Harper J. F. (2002). Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130, 2129–2141. 10.1104/pp.008532 PubMed DOI PMC
Kumar M., Gouw M., Michael S., Sámano-Sánchez H., Pancsa R., Glavina J., et al. . (2020). ELM-the eukaryotic linear motif resource in 2020. Nucleic Acids Res. 48, D296–D306. 10.1093/nar/gkz1030 PubMed DOI PMC
Kumar S., Sud N., Fonseca F. V., Hou Y., Black S. M. (2010). Shear stress stimulates nitric oxide signaling in pulmonary arterial endothelial cells via a reduction in catalase activity: role of protein kinase C delta. Am. J. Physiol. Lung Cell Mol. Physiol. 298, L105–L116. 10.1152/ajplung.00290.2009 PubMed DOI PMC
Kuo W. Y., Huang C. H., Liu A. C., Cheng C. P., Li S. H., Chang W. C., et al. . (2013). CHAPERONIN 20 mediates iron superoxide dismutase (FeSOD) activity independent of its co-chaperonin role in Arabidopsis chloroplasts. New Phytol. 197, 99–110. 10.1111/j.1469-8137.2012.04369.x PubMed DOI
Lehmann S., Serrano M., L'Haridon F., Tjamos S. E., Metraux J.-P. (2015). Reactive oxygen species and plant resistance to fungal pathogens. Phytochemistry 112, 54–62. 10.1016/j.phytochem.2014.08.027 PubMed DOI
Leitch J. M., Li C. X., Baron J. A., Matthews L. M., Cao X., Hart P. J., et al. . (2012). Post-translational modification of Cu/Zn superoxide dismutase under anaerobic conditions. Biochemistry 51, 677–685. 10.1021/bi201353y PubMed DOI PMC
Li H., Wong W. S., Zhu L., Guo H. W., Ecker J., Li N. (2009). Phosphoproteomic analysis of ethylene-regulated protein phosphorylation in etiolated seedlings of Arabidopsis mutant ein2 using two-dimensional separations coupled with a hybrid quadrupole time-of-flight mass spectrometer. Proteomics 9, 1646–1661. 10.1002/pmic.200800420 PubMed DOI
Li X., Makavitskaya M., Samokhina V., Mackievic V., Navaselsky I., Hryvusevich P., et al. . (2018). Effects of exogenously-applied L-ascorbic acid on root expansive growth and viability of the border-like cells. Plant Signal. Behav. 13:e1514895. 10.1080/15592324.2018.1514895 PubMed DOI PMC
Lin F., Ding H., Wang J., Zhang H., Zhang A., Zhang Y., et al. . (2009). Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J. Exp. Bot. 60, 3221–3238. 10.1093/jxb/erp157 PubMed DOI PMC
Lin L. L., Hsu C. L., Hu C. W., Ko S. Y., Hsieh H. L., Huang H. C., et al. . (2015). Integrating phosphoproteomics and bioinformatics to study brassinosteroid-regulated phosphorylation dynamics in Arabidopsis. BMC Genom. 16, 533. 10.1186/s12864-015-1753-4 PubMed DOI PMC
Lindermayr C. (2018). Crosstalk between reactive oxygen species and nitric oxide in plants: key role of S-nitrosoglutathione reductase. Free Radic. Biol. Med. 122, 110–115. 10.1016/j.freeradbiomed.2017.11.027 PubMed DOI
Lindermayr C., Durner J. (2015). Interplay of reactive oxygen species and nitric oxide: nitric oxide coordinates reactive oxygen species homeostasis. Plant Physiol. 167, 1209–1210. 10.1104/pp.15.00293 PubMed DOI PMC
Lisenbee C. S., Lingard M. J., Trelease R. N. (2005). Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase. Plant J. 43, 900–914. 10.1111/j.1365-313X.2005.02503.x PubMed DOI
Liu P., Sun F., Gao R., Dong H. (2012). RAP2.6L overexpression delays waterlogging induced premature senescence by increasing stomatal closure more than antioxidant enzyme activity. Plant Mol. Biol. 79, 609–622. 10.1007/s11103-012-9936-8 PubMed DOI
Liu Y., He C. (2017). A review of redox signaling and the control of MAP kinase pathway in plants. Redox Biol. 11, 192–204. 10.1016/j.redox.2016.12.009 PubMed DOI PMC
Locato V., Cimini S., De Gara L. (2017). Glutathione as a key player in plant abiotic stress responses and tolerance, in Glutathione in Plant Growth, Development, and Stress Tolerance, eds M. A. Hossain, M. G. Mostofa, P. Diaz-Vivancos, D. J. Burritt, M. Fujita, and L.-S. P. Tran (Cham: Springer International Publishing: ), 127–145. 10.1007/978-3-319-66682-2_6 DOI
Ma C., Burd S., Lers A. (2015). miR408 is involved in abiotic stress responses in Arabidopsis. Plant J. 84, 169–187. 10.1111/tpj.12999 PubMed DOI
Marcec M. J., Gilroy S., Poovaiah B. W., Tanaka K. (2019). Mutual interplay of Ca2+ and ROS signaling in plant immune response. Plant Sci. 283, 343–354. 10.1016/j.plantsci.2019.03.004 PubMed DOI
Marchand C. H., Vanacker H., Collin V., Issakidis-Bourguet E., Maréchal P. L., Decottignies P. (2010). Thioredoxin targets in Arabidopsis roots. Proteomics 10, 2418–2428. 10.1002/pmic.200900835 PubMed DOI
Marty L., Bausewein D., Müller C., Bangash S., Moseler A., Schwarzländer M., et al. . (2019). Arabidopsis glutathione reductase 2 is indispensable in plastids, while mitochondrial glutathione is safeguarded by additional reduction and transport systems. New Phytol. 224, 1569–1584. 10.1111/nph.16086 PubMed DOI
Maruta T., Inoue T., Noshi M., Tamoi M., Yabuta Y., Yoshimura K., et al. . (2012). Cytosolic ascorbate peroxidase 1 protects organelles against oxidative stress by wounding- and jasmonate-induced H2O2 in Arabidopsis plants. Biochim. Biophys. Acta 1820, 1901–1907. 10.1016/j.bbagen.2012.08.003 PubMed DOI
Maruta T., Sawa Y., Shigeoka S., Ishikawa T. (2016). Diversity and evolution of ascorbate peroxidase functions in chloroplasts: more than just a classical antioxidant enzyme? Plant Cell Physiol. 57, 1377–1386. 10.1093/pcp/pcv203 PubMed DOI
Maruta T., Tanouchi A., Tamoi M., Yabuta Y., Yoshimura K., Ishikawa T., et al. . (2010). Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol. 51, 190–200. 10.1093/pcp/pcp177 PubMed DOI
Mayank P., Grossman J., Wuest S., Boisson-Dernier A., Roschitzki B., Nanni P., et al. . (2012). Characterization of the phosphoproteome of mature Arabidopsis pollen. Plant J. 72, 89–101. 10.1111/j.1365-313X.2012.05061.x PubMed DOI
Meyer A. J., Dreyer A., Ugalde J. M., Feitosa-Araujo E., Dietz K.-J., Schwarzländer M. (in press). Shifting paradigms novel players in Cys-based redox regulation ROS signaling in plants - where to go next. Biol. Chem. 10.1515/hsz-2020-0291 PubMed DOI
Mhamdi A., Noctor G., Baker A. (2012). Plant catalases: peroxisomal redox guardians. Arch. Biochem. Biophys. 525, 181–194. 10.1016/j.abb.2012.04.015 PubMed DOI
Mhamdi A., Queval G., Chaouch S., Vanderauwera S., Van Breusegem F., Noctor G. (2010). Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J. Exp. Bot. 61, 4197–4220. 10.1093/jxb/erq282 PubMed DOI
Mhamdi A., Van Breusegem F. (2018). Reactive oxygen species in plant development. Development 145:dev164376. 10.1242/dev.164376 PubMed DOI
Miao Y., Laun T., Zimmermann P., Zentgraf U. (2004). Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol. Biol. 55, 853–867. 10.1007/s11103-004-2142-6 PubMed DOI
Miao Y., Laun T. M., Smykowski A., Zentgraf U. (2007). Arabidopsis MEKK1 can take a short cut: it can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter. Plant Mol. Biol. 65, 63–76. 10.1007/s11103-007-9198-z PubMed DOI
Mignolet-Spruyt L., Xu E., Idänheimo N., Hoeberichts F. A., Mühlenbock P., Brosché M., et al. . (2016). Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J. Exp. Bot. 67, 3831–3844. 10.1093/jxb/erw080 PubMed DOI
Miller E. W., Dickinson B. C., Chang C. J. (2010). Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc. Natl. Acad. Sci. U.S.A. 107, 15681–15686. 10.1073/pnas.1005776107 PubMed DOI PMC
Mithoe S. C., Boersema P. J., Berke L., Snel B., Heck A. J., Menke F. L. (2012). Targeted quantitative phosphoproteomics approach for the detection of phospho-tyrosine signaling in plants. J. Proteome Res. 11, 438–448. 10.1021/pr200893k PubMed DOI
Mittler R. (2017). ROS are good. Trends Plant Sci. 22, 11–19. 10.1016/j.tplants.2016.08.002 PubMed DOI
Mittler R., Kim Y., Song L., Coutu J., Coutu A., Ciftci-Yilmaz S., et al. . (2006). Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett. 580, 6537–6542. 10.1016/j.febslet.2006.11.002 PubMed DOI PMC
Mittler R., Vanderauwera S., Suzuki N., Miller G., Tognetti V. B., Vandepoele K., et al. . (2011). ROS signaling: the new wave? Trends Plant Sci. 16, 300–309. 10.1016/j.tplants.2011.03.007 PubMed DOI
Morgan M. J., Lehmann M., Schwarzländer M., Baxter C. J., Sienkiewicz-Porzucek A., Williams T. C., et al. . (2008). Decrease in manganese superoxide dismutase leads to reduced root growth and affects tricarboxylic acid cycle flux and mitochondrial redox homeostasis. Plant Physiol. 147, 101–114. 10.1104/pp.107.113613 PubMed DOI PMC
Müller-Schüssele S. J., Wang R., Gütle D. D., Romer J., Rodriguez-Franco M., Scholz M., et al. . (2020). Chloroplasts require glutathione reductase to balance reactive oxygen species and maintain efficient photosynthesis. Plant J. 103, 1140–1154. 10.1111/tpj.14791 PubMed DOI
Muñoz P., Munné-Bosch S. (2019). Vitamin E in plants: biosynthesis, transport, and function. Trends Plant Sci. 24, 1040–1051. 10.1016/j.tplants.2019.08.006 PubMed DOI
Murgia I., Tarantino D., Vannini C., Bracale M., Carravieri S., Soave C. (2004). Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to Paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J. 38, 940–953. 10.1111/j.1365-313X.2004.02092.x PubMed DOI
Myouga F., Hosoda C., Umezawa T., Iizumi H., Kuromori T., Motohashi R., et al. . (2008). A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 20, 3148–3162. 10.1105/tpc.108.061341 PubMed DOI PMC
Nakagami H., Soukupová H., Schikora A., Zárský V., Hirt H. (2006). A Mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J. Biol. Chem. 281, 38697–38704. 10.1074/jbc.M605293200 PubMed DOI
Nakagami H., Sugiyama N., Mochida K., Daudi A., Yoshida Y., Toyoda T., et al. . (2010). Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. J. Plant Physiol. 153, 1161–1174. 10.1104/pp.110.157347 PubMed DOI PMC
Narendra S., Venkataramani S., Shen G., Wang J., Pasapula V., Lin Y., et al. . (2006). The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J. Exp. Bot. 57, 3033–3042. 10.1093/jxb/erl060 PubMed DOI
Niu L., Liao W. (2016). Hydrogen peroxide signaling in plant development and abiotic responses: crosstalk with nitric oxide and calcium. Front Plant Sci. 7:230. 10.3389/fpls.2016.00230 PubMed DOI PMC
Noctor G., Reichheld J.-P., Foyer C. H. (2017). ROS-related redox regulation and signaling in plants. Cell Dev. Biol. 80, 3–12. 10.1016/j.semcdb.2017.07.013 PubMed DOI
Noshi M., Hatanaka R., Tanabe N., Terai Y., Maruta T., Shigeoka S. (2016). Redox regulation of ascorbate and glutathione by a chloroplastic dehydroascorbate reductase is required for high-light stress tolerance in Arabidopsis. Biosci. Biotechnol. Biochem. 80, 870–877. 10.1080/09168451.2015.1135042 PubMed DOI
Noshi M., Yamada H., Hatanaka R., Tanabe N., Tamoi M., Shigeoka S. (2017). Arabidopsis dehydroascorbate reductase 1 and 2 modulate redox states of ascorbate-glutathione cycle in the cytosol in response to photooxidative stress. Biosci. Biotechnol. Biochem. 81, 523–533. 10.1080/09168451.2016.1256759 PubMed DOI
Obara K., Sumi K., Fukuda H. (2002). The use of multiple transcription starts causes the dual targeting of Arabidopsis putative monodehydroascorbate reductase to both mitochondria and chloroplasts. Plant Cell Physiol. 43, 697–705. 10.1093/pcp/pcf103 PubMed DOI
Obayashi T., Aoki Y., Tadaka S., Kagaya Y., Kinoshita K. (2018). ATTED-II in 2018: a plant coexpression database based on investigation of the statistical property of the mutual rank index. Plant Cell Physiol. 59:e3 10.1093/pcp/pcx191 PubMed DOI PMC
Ono M., Isono K., Sakata Y., Taji T. (2020). CATALASE2 plays a crucial role in long-term heat tolerance of Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 534, 747–751. 10.1016/j.bbrc.2020.11.006 PubMed DOI
Ortega-Galisteo A. P., Rodríguez-Serrano M., Pazmiño D. M., Gupta D. K., Sandalio L. M., Romero-Puertas M. C. (2012). S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J. Exp. Bot. 63, 2089–2103. 10.1093/jxb/err414 PubMed DOI PMC
Ortiz-Masia D., Perez-Amador M. A., Carbonell J., Marcote M. J. (2007). Diverse stress signals activate the C1 subgroup MAP kinases of Arabidopsis. FEBS Lett. 581, 1834–1840. 10.1016/j.febslet.2007.03.075 PubMed DOI
Palma J. M., Mateos R. M., López-Jaramillo J., Rodríguez-Ruiz M., González-Gordo S., Lechuga-Sancho A. M., et al. . (2020). Plant catalases as NO and H2S targets. Redox Biol. 34:101525. 10.1016/j.redox.2020.101525 PubMed DOI PMC
Pandey S., Fartyal D., Agarwal A., Shukla T., James D., Kaul T., et al. . (2017). Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Front. Plant Sci. 8:581. 10.3389/fpls.2017.00581 PubMed DOI PMC
Pasternak T. P., Ötvös K., Domoki M., Fehér A. (2007). Linked activation of cell division and oxidative stress defense in alfalfa leaf protoplast-derived cells is dependent on exogenous auxin. Plant Growth Regul. 51, 109–117. 10.1007/s10725-006-9152-0 DOI
Pei Z.-M., Murata Y., Benning G., Thomine S., Klüsener B., Allen G. J., et al. . (2000). Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406, 731–734. 10.1038/35021067 PubMed DOI
Perea-García A., Andrés-Bordería A., Mayo de Andrés S., Sanz A., Davis A. M., Davis S., et al. . (2016). Modulation of copper deficiency responses by diurnal and circadian rhythms in Arabidopsis thaliana. J. Exp. Bot. 67, 391–403. 10.1093/jxb/erv474 PubMed DOI PMC
Pérez-Salamó I., Papdi C., Rigó G., Zsigmond L., Vilela B., Lumbreras V., et al. . (2014). The heat shock factor A4A confers salt tolerance and is regulated by oxidative stress and the mitogen-activated protein kinases MPK3 and MPK6. Plant Physiol. 165, 319–334. 10.1104/pp.114.237891 PubMed DOI PMC
Persak H., Pitzschke A. (2013). Tight interconnection and multi-level control of Arabidopsis MYB44 in MAPK cascade signalling. PLoS ONE 8:e57547. 10.1371/journal.pone.0057547 PubMed DOI PMC
Persak H., Pitzschke A. (2014). Dominant repression by Arabidopsis transcription factor MYB44 causes oxidative damage and hypersensitivity to abiotic stress. Int. J. Mol. Sci. 15, 2517–2537. 10.3390/ijms15022517 PubMed DOI PMC
Petrov V., Hille J., Mueller-Roeber B., Gechev T. S. (2015). ROS-mediated abiotic stress-induced programmed cell death in plants. Front. Plant Sci. 6:69. 10.3389/fpls.2015.00069 PubMed DOI PMC
Pilon M. (2017). The copper microRNAs. New Phytol. 213, 1030–1035. 10.1111/nph.14244 PubMed DOI
Pilon M., Ravet K., Tapken W. (2011). The biogenesis and physiological function of chloroplast superoxide dismutases. Biochim. Biophys. Acta 1807, 989–998. 10.1016/j.bbabio.2010.11.002 PubMed DOI
Piterková J., Luhová L., Navrátilová B., Sedlárová M., Petrivalsky M. (2015). Early and long-term responses of cucumber cells to high cadmium concentration are modulated by nitric oxide and reactive oxygen species. Acta Physiol. Plant 37:19 10.1007/s11738-014-1756-9 DOI
Pitzschke A., Djamei A., Bitton F., Hirt H. (2009). A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol. Plant 2, 120–137. 10.1093/mp/ssn079 PubMed DOI PMC
Pnueli L., Liang H., Rozenberg M., Mittler R. (2003). Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J. 34, 187–203. 10.1046/j.1365-313x.2003.01715.x PubMed DOI
Pospíšil P. (2016). Production of reactive oxygen species by photosystem II as a response to light and temperature stress. Front. Plant Sci. 7:1950. 10.3389/fpls.2016.01950 PubMed DOI PMC
Rafikov R., Kumar S., Aggarwal S., Hou Y., Kangath A., Pardo D., et al. . (2014). Endothelin-1 stimulates catalase activity through the PKCδ-mediated phosphorylation of serine 167. Free Radic. Biol. Med. 67, 255–264. 10.1016/j.freeradbiomed.2013.10.814 PubMed DOI PMC
Rahantaniaina M.-S., Li S., Chatel-Innocenti G., Tuzet A., Issakidis-Bourguet E., Mhamdi A., et al. . (2017). Cytosolic and chloroplastic DHARs cooperate in oxidative stress-driven activation of the salicylic acid pathway. Plant Physiol. 174, 956–971. 10.1104/pp.17.00317 PubMed DOI PMC
Rahman A., Mostofa M. G., Alam M. M., Nahar K., Hasanuzzaman M., Fujita M. (2015). Calcium mitigates arsenic toxicity in rice seedlings by reducing arsenic uptake and modulating the antioxidant defense and glyoxalase systems and stress markers. Biomed Res. Int. 2015:340812. 10.1155/2015/340812 PubMed DOI PMC
Rayapuram N., Bigeard J., Alhoraibi H., Bonhomme L., Hesse A. M., Vinh J., et al. . (2018). Quantitative phosphoproteomic analysis reveals shared and specific targets of Arabidopsis mitogen-activated protein kinases (MAPKs) MPK3, MPK4, and MPK6. Mol. Cell. Proteom. 17, 61–80. 10.1074/mcp.RA117.000135 PubMed DOI PMC
Rayapuram N., Bonhomme L., Bigeard J., Haddadou K., Przybylski C., Hirt H., et al. . (2014). Identification of novel PAMP-triggered phosphorylation and dephosphorylation events in Arabidopsis thaliana by quantitative phosphoproteomic analysis. J. Proteome Res. 13, 2137–2151. 10.1021/pr401268v PubMed DOI
Reiland S., Finazzi G., Endler A., Willig A., Baerenfaller K., Grossmann J., et al. . (2011). Comparative phosphoproteome profiling reveals a function of the STN8 kinase in fine-tuning of cyclic electron flow (CEF). Proc. Natl. Acad. Sci. U.S.A. 108, 12955–12960. 10.1073/pnas.1104734108 PubMed DOI PMC
Reiland S., Messerli G., Baerenfaller K., Gerrits B., Endler A., Grossmann J., et al. . (2009). Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol. 150, 889–903. 10.1104/pp.109.138677 PubMed DOI PMC
Rentel M. C., Lecourieux D., Ouaked F., Usher S. L., Petersen L., Okamoto H., et al. . (2004). OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427, 858–861. 10.1038/nature02353 PubMed DOI
Richards S. L., Laohavisit A., Mortimer J. C., Shabala L., Swarbreck S. M., Shabala S., et al. . (2014). Annexin 1 regulates the H2O2-induced calcium signature in Arabidopsis thaliana roots. Plant J. 77, 136–145. 10.1111/tpj.12372 PubMed DOI
Riester L., Köster-Hofmann S., Doll J., Berendzen K. W., Zentgraf U. (2019). Impact of alternatively polyadenylated isoforms of ETHYLENE RESPONSE FACTOR4 with activator and repressor function on senescence in Arabidopsis thaliana L. Genes 10:91. 10.3390/genes10020091 PubMed DOI PMC
Rizhsky L., Davletova S., Liang H., Mittler R. (2004b). The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J. Biol. Chem. 279, 11736–11743. 10.1074/jbc.M313350200 PubMed DOI
Rizhsky L., Liang H., Mittler R. (2003). The water-water cycle is essential for chloroplast protection in the absence of stress. J. Biol. Chem. 278, 38921–38925. 10.1074/jbc.M304987200 PubMed DOI
Rizhsky L., Liang H., Shuman J., Shulaev V., Davletova S., Mittler R. (2004a). When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 134, 1683–1696. 10.1104/pp.103.033431 PubMed DOI PMC
Rizwan M., Mostofa M. G., Ahmad M. Z., Imtiaz M., Mehmood S., Adeel M., et al. . (2018). Nitric oxide induces rice tolerance to excessive nickel by regulating nickel uptake, reactive oxygen species detoxification and defense-related gene expression. Chemosphere 191, 23–35. 10.1016/j.chemosphere.2017.09.068 PubMed DOI
Roitinger E., Hofer M., Köcher T., Pichler P., Novatchkova M., Yang J., et al. . (2015). Quantitative phosphoproteomics of the ataxia telangiectasia-mutated (ATM) and ataxia telangiectasia-mutated and rad3-related (ATR) dependent DNA damage response in Arabidopsis thaliana. Mol. Cell Proteomics 14, 556–571. 10.1074/mcp.M114.040352 PubMed DOI PMC
Romeis T., Herde M. (2014). From local to global: CDPKs in systemic defense signaling upon microbial and herbivore attack. Curr. Opin. Plant Biol. 20, 1–10. 10.1016/j.pbi.2014.03.002 PubMed DOI
Romero-Puertas M. C., Sandalio L. M. (2016). Nitric oxide level is self-regulating and also regulates its ROS partners. Front. Plant Sci. 7:316. 10.3389/fpls.2016.00316 PubMed DOI PMC
Rossel J. B., Walter P. B., Hendrickson L., Chow W. S., Poole A., Mullineaux P. M., et al. . (2006). A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance. Plant Cell Environ. 29, 269–281. 10.1111/j.1365-3040.2005.01419.x PubMed DOI
Rudnik R., Bulcha J. T., Reifschneider E., Ellersiek U., Baier M. (2017). Specificity versus redundancy in the RAP2.4 transcription factor family of Arabidopsis thaliana: transcriptional regulation of genes for chloroplast peroxidases. BMC Plant Biol. 17:144. 10.1186/s12870-017-1092-5 PubMed DOI PMC
Ruiz-May E., Segura-Cabrera A., Elizalde-Contreras J. M., Shannon L. M., Loyola-Vargas V. M. (2019). A recent advance in the intracellular and extracellular redox post-translational modification of proteins in plants. J. Mol. Recogn. 32:e2754. 10.1002/jmr.2754 PubMed DOI
Sagi M., Fluhr R. (2006). Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol. 141, 336–340. 10.1104/pp.106.078089 PubMed DOI PMC
Šamajová O., Plíhal O., Al-Yousif M., Hirt H., Šamaj J. (2013). Improvement of stress tolerance in plants by genetic manipulation of mitogen-activated protein kinases. Biotechnol. Adv. 31, 118–128. 10.1016/j.biotechadv.2011.12.002 PubMed DOI
Savatin D. V., Bisceglia N. G., Marti L., Fabbri C., Cervone F., De Lorenzo G. (2014). The Arabidopsis NUCLEUS- AND PHRAGMOPLAST-LOCALIZED KINASE1-related protein kinases are required for elicitor-induced oxidative burst and immunity. Plant Physiol. 165, 1188–1202. 10.1104/pp.114.236901 PubMed DOI PMC
Schopfer P., Liszkay A., Bechtold M., Frahry G., Wagner A. (2002). Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214, 821–828. 10.1007/s00425-001-0699-8 PubMed DOI
Schulz P., Herde M., Romeis T. (2013). Calcium-dependent protein kinases: hubs in plant stress signaling and development. Plant Physiol. 163, 523–530. 10.1104/pp.113.222539 PubMed DOI PMC
Sewelam N., Kazan K., Thomas-Hall S. R., Kidd B. N., Manners J. M., Schenk P. M. (2013). Ethylene response factor 6 is a regulator of reactive oxygen species signaling in Arabidopsis. PLoS ONE 8:e70289. 10.1371/journal.pone.0070289 PubMed DOI PMC
Shafi A., Chauhan R., Gill T., Swarnkar M. K., Sreenivasulu Y., Kumar S., et al. . (2015). Expression of SOD and APX genes positively regulates secondary cell wall biosynthesis and promotes plant growth and yield in Arabidopsis under salt stress. Plant Mol. Biol. 87, 615–631. 10.1007/s11103-015-0301-6 PubMed DOI
Shaikhali J., Heiber I., Seidel T., Ströher E., Hiltscher H., Birkmann S., et al. . (2008). The redox-sensitive transcription factor Rap2.4a controls nuclear expression of 2-Cys peroxiredoxin A and other chloroplast antioxidant enzymes. BMC Plant Biol. 8:48. 10.1186/1471-2229-8-48 PubMed DOI PMC
Shan C., Yang T. (2017). Nitric oxide acts downstream of hydrogen peroxide in the regulation of ascorbate and glutathione metabolism by jasmonic acid in Agropyron cristatum leaves. Biol. Plant. 61, 779–784. 10.1007/s10535-017-0708-9 DOI
Shapiguzov A., Vainonen J. P., Hunter K., Tossavainen H., Tiwari A., Järvi S., et al. . (2019). Arabidopsis RCD1 coordinates chloroplast and mitochondrial functions through interaction with ANAC transcription factors. Elife 8:e43284. 10.7554/eLife.43284 PubMed DOI PMC
Sharma I., Ahmad P. (2014). Catalase: a versatile antioxidant in plants, in Oxidative Damage to Plants, ed P. Ahmad (Srinagar: S.P. College; ), 131–148.
Shukla P., Singh A. K. (2015). Nitric oxide mitigates arsenic-induced oxidative stress and genotoxicity in Vicia faba L. Environ. Sci. Pollut. Res. 22, 13881–13891. 10.1007/s11356-015-4501-z PubMed DOI
Sierla M., Waszczak C., Vahisalu T., Kangasjärvi J. (2016). Reactive oxygen species in the regulation of stomatal movements. Plant Physiol. 171, 1569–1580. 10.1104/pp.16.00328 PubMed DOI PMC
Smékalová V., Doskočilová A., Komis G., Šamaj J. (2014). Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechnol. Adv. 32, 2–11. 10.1016/j.biotechadv.2013.07.009 PubMed DOI
Smirnoff N. (2018). Ascorbic acid metabolism and functions: a comparison of plants and mammals. Free Radic. Biol. Med. 122, 116–129. 10.1016/j.freeradbiomed.2018.03.033 PubMed DOI PMC
Smirnoff N., Arnaud D. (2019). Hydrogen peroxide metabolism and functions in plants. New Phytol. 221, 1197–1214. 10.1111/nph.15488 PubMed DOI
Song C., Chung W. S., Lim C. O. (2016). Overexpression of heat shock factor gene HsfA3 increases galactinol levels and oxidative stress tolerance in Arabidopsis. Mol. Cells 39, 477–483. 10.14348/molcells.2016.0027 PubMed DOI PMC
Su T., Wang P., Li H., Zhao Y., Lu Y., Dai P., et al. . (2018). The Arabidopsis catalase triple mutant reveals important roles of catalases and peroxisome-derived signaling in plant development. J. Integr. Plant Biol. 60, 591–607. 10.1111/jipb.12649 PubMed DOI
Sugiyama N., Nakagami H., Mochida K., Daudi A., Tomita M., Shirasu K., et al. . (2008). Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Mol. Syst. Biol. 4:193. 10.1038/msb.2008.32 PubMed DOI PMC
Sultana S., Khew C. Y., Morshed M. M., Namasivayam P., Napis S., Ho C. L. (2012). Overexpression of monodehydroascorbate reductase from a mangrove plant (AeMDHAR) confers salt tolerance on rice. J. Plant Physiol. 169, 311–318. 10.1016/j.jplph.2011.09.004 PubMed DOI
Sumugat M. R., Donahue J. L., Cortes D. F., Stromberg V. K., Grene R., Shulaev V., et al. (2010). Seed development and germination in an Arabidopsis thaliana line antisense to glutathione reductase 2. J. New Seeds 11, 104–126. 10.1080/15228861003776175 DOI
Sunkar R., Kapoor A., Zhu J. K. (2006). Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18, 2051–2065. 10.1105/tpc.106.041673 PubMed DOI PMC
Suzuki N., Miller G., Sejima H., Harper J., Mittler R. (2013). Enhanced seed production under prolonged heat stress conditions in Arabidopsis thaliana plants deficient in cytosolic ascorbate peroxidase 2. J. Exp. Bot. 64, 253–263. 10.1093/jxb/ers335 PubMed DOI PMC
Suzuki Y. J., Carini M., Butterfield D. A. (2010). Protein carbonylation. Antioxid. Redox Signal. 12, 323–325. 10.1089/ars.2009.2887 PubMed DOI PMC
Takáč T., Obert B., Rolčík J., Šamaj J. (2016a). Improvement of adventitious root formation in flax using hydrogen peroxide. N. Biotechnol. 33, 728–734. 10.1016/j.nbt.2016.02.008 PubMed DOI
Takáč T., Šamajová O., Vadovič P., Pechan T., Košútová P., Ovečka M., et al. . (2014). Proteomic and biochemical analyses show a functional network of proteins involved in antioxidant defense of the Arabidopsis anp2anp3 double mutant. J. Proteome Res. 13, 5347–5361. 10.1021/pr500588c PubMed DOI PMC
Takáč T., Vadovič P., Pechan T., Luptovčiak I., Šamajová O., Šamaj J. (2016b). Comparative proteomic study of Arabidopsis mutants mpk4 and mpk6. Sci. Rep. 6:28306. 10.1038/srep28306 PubMed DOI PMC
Teh O.-K., Hofius D. (2014). Membrane trafficking and autophagy in pathogen-triggered cell death and immunity. J. Exp. Bot. 65, 1297–1312. 10.1093/jxb/ert441 PubMed DOI
Tian W., Wang C., Gao Q., Li L., Luan S. (2020). Calcium spikes, waves and oscillations in plant development and biotic interactions. Nat. Plants 6, 750–759. 10.1038/s41477-020-0667-6 PubMed DOI
Tichá T., Lochman J., Cinčalová L., Luhová L., Petrivalský M. (2017). Redox regulation of plant S-nitrosoglutathione reductase activity through post-translational modifications of cysteine residues. Biochem. Biophys. Res. Commun. 494, 27–33. 10.1016/j.bbrc.2017.10.090 PubMed DOI
Tognetti V. B., Van Aken O., Morreel K., Vandenbroucke K., van de Cotte B., De Clercq I., et al. . (2010). Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell 22, 2660–2679. 10.1105/tpc.109.071316 PubMed DOI PMC
Tsang C. K., Chen M., Cheng X., Qi Y., Chen Y., Das I., et al. . (2018). SOD1 phosphorylation by mTORC1 couples nutrient sensing and redox regulation. Mol. Cell 70, 502–515.e8. 10.1016/j.molcel.2018.03.029 PubMed DOI PMC
Tsang C. K., Liu Y., Thomas J., Zhang Y., Zheng X. F. (2014). Superoxide dismutase 1 acts as a nuclear transcription factor to regulate oxidative stress resistance. Nat. Commun. 5:3446. 10.1038/ncomms4446 PubMed DOI PMC
Tuzet A., Rahantaniaina M. S., Noctor G. (2019). Analyzing the function of catalase and the ascorbate-glutathione pathway in H2O2 processing: insights from an experimentally constrained kinetic model. Antioxid. Redox Signal. 30, 1238–1268. 10.1089/ars.2018.7601 PubMed DOI
Umezawa T., Sugiyama N., Takahashi F., Anderson J. C., Ishihama Y., Peck S. C., et al. . (2013). Genetics and phosphoproteomics reveal a protein phosphorylation network in the abscisic acid signaling pathway in Arabidopsis thaliana. Sci. Signal. 6:rs8. 10.1126/scisignal.2003509 PubMed DOI
Ushimaru T., Nakagawa T., Fujioka Y., Daicho K., Naito M., Yamauchi Y., et al. . (2006). Transgenic Arabidopsis plants expressing the rice dehydroascorbate reductase gene are resistant to salt stress. J. Plant Physiol. 163, 1179–1184. 10.1016/j.jplph.2005.10.002 PubMed DOI
Vadassery J., Tripathi S., Prasad R., Varma A., Oelmüller R. (2009). Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. J. Plant Physiol. 166, 1263–1274. 10.1016/j.jplph.2008.12.016 PubMed DOI
van Buer J., Cvetkovic J., Baier M. (2016). Cold regulation of plastid ascorbate peroxidases serves as a priming hub controlling ROS signaling in Arabidopsis thaliana. BMC Plant Biol. 16:163. 10.1186/s12870-016-0856-7 PubMed DOI PMC
Van Leene J., Han C., Gadeyne A., Eeckhout D., Matthijs C., Cannoot B., et al. . (2019). Capturing the phosphorylation and protein interaction landscape of the plant TOR kinase. Nat. Plants 5, 316–327. 10.1038/s41477-019-0378-z PubMed DOI
Vandenabeele S., Vanderauwera S., Vuylsteke M., Rombauts S., Langebartels C., Seidlitz H. K., et al. . (2004). Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J. 39, 45–58. 10.1111/j.1365-313X.2004.02105.x PubMed DOI
Vanderauwera S., Suzuki N., Miller G., van de Cotte B., Morsa S., Ravanat J. L., et al. . (2011). Extranuclear protection of chromosomal DNA from oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 108, 1711–1716. 10.1073/pnas.101835910 PubMed DOI PMC
Vogel J. T., Zarka D. G., Van Buskirk H. A., Fowler S. G., Thomashow M. F. (2005). Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J. 41, 195–211. 10.1111/j.1365-313X.2004.02288.x PubMed DOI
Vogel M. O., Moore M., König K., Pecher P., Alsharafa K., Lee J., et al. . (2014). Fast retrograde signaling in response to high light involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF transcription factors in Arabidopsis. Plant cell 26, 1151–1165. 10.1105/tpc.113.121061 PubMed DOI PMC
Voothuluru P., Sharp R. E. (2013). Apoplastic hydrogen peroxide in the growth zone of the maize primary root under water stress. I. Increased levels are specific to the apical region of growth maintenance. J. Exp. Bot. 64, 1223–1233. 10.1093/jxb/ers277 PubMed DOI
Vu L. D., Gevaert K., De Smet I. (2018). Protein language: post-translational modifications talking to each other. Trends Plant Sci. 23, 1068–1080. 10.1016/j.tplants.2018.09.004 PubMed DOI
Wang B., Ding H., Chen Q., Ouyang L., Li S., Zhang J. (2019). Enhanced tolerance to methyl viologen-mediated oxidative stress via AtGR2 expression from chloroplast genome. Front. Plant Sci. 10:1178. 10.3389/fpls.2019.01178 PubMed DOI PMC
Wang P., Du Y., Zhao X., Miao Y., Song C. P. (2013a). The MPK6-ERF6-ROS-responsive cis-acting Element7/GCC box complex modulates oxidative gene transcription and the oxidative response in Arabidopsis. Plant Physiol. 161, 1392–1408. 10.1104/pp.112.210724 PubMed DOI PMC
Wang P., Xue L., Batelli G., Lee S., Hou Y. J., Van Oosten M. J., et al. . (2013b). Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action. Proc. Natl. Acad. Sci. U.S.A. 110, 11205–11210. 10.1073/pnas.1308974110 PubMed DOI PMC
Wang W., Zhang H., Wei X., Yang L., Yang B., Zhang L., et al. . (2018). Functional characterization of calcium-dependent protein kinase (CPK) 2 gene from oilseed rape (Brassica napus L.) in regulating reactive oxygen species signaling and cell death control. Gene 651, 49–56. 10.1016/j.gene.2018.02.006 PubMed DOI
Wang X., Bian Y., Cheng K., Gu L. F., Ye M., Zou H., et al. . (2013c). A large-scale protein phosphorylation analysis reveals novel phosphorylation motifs and phosphoregulatory networks in Arabidopsis. J. Proteom. 78, 486–498. 10.1016/j.jprot.2012.10.018 PubMed DOI
Wang X., Bian Y., Cheng K., Zou H., Sun S. S., He J. X. (2012). A comprehensive differential proteomic study of nitrate deprivation in Arabidopsis reveals complex regulatory networks of plant nitrogen responses. J. Proteome Res. 11, 2301–2315. 10.1021/pr2010764 PubMed DOI
Wang Z., Xiao Y., Chen W., Tang K., Zhang L. (2010). Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis. J. Integr. Plant Biol. 52, 400–409. 10.1111/j.1744-7909.2010.00921.x PubMed DOI
Waszczak C., Akter S., Eeckhout D., Persiau G., Wahni K., Bodra N., et al. . (2014). Sulfenome mining in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 111, 11545–11550. 10.1073/pnas.1411607111 PubMed DOI PMC
Waszczak C., Akter S., Jacques S., Huang J., Messens J., Van Breusegem F. (2015). Oxidative post-translational modifications of cysteine residues in plant signal transduction. J. Exp. Bot. 66, 2923–2934. 10.1093/jxb/erv084 PubMed DOI
Waszczak C., Carmody M., Kangasjärvi J. (2018). Reactive oxygen species in plant signaling. Annu. Rev. Plant Biol. 69, 209–236. 10.1146/annurev-arplant-042817-040322 PubMed DOI
Wen F., Ye F., Xiao Z., Liao L., Li T., Jia M., et al. . (2020). Genome-wide survey and expression analysis of calcium-dependent protein kinase (CDPK) in grass Brachypodium distachyon. BMC Genomics 21:53. 10.1186/s12864-020-6475-6 PubMed DOI PMC
Withers J., Dong X. (2017). Post-translational regulation of plant immunity. Curr. Opin. Plant Biol. 38, 124–132. 10.1016/j.pbi.2017.05.004 PubMed DOI PMC
Wu F., Chi Y., Jiang Z., Xu Y., Xie L., Huang F., et al. . (2020). Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature 578, 577–581. 10.1038/s41586-020-2032-3 PubMed DOI
Wu T. M., Lin W. R., Kao C. H., Hong C. Y. (2015). Gene knockout of glutathione reductase 3 results in increased sensitivity to salt stress in rice. Plant Mol. Biol. 87, 555–564. 10.1007/s11103-015-0290-5 PubMed DOI
Xia X.-J., Zhou Y.-H., Shi K., Zhou J., Foyer C. H., Yu J.-Q. (2015). Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J. Exp. Bot. 66, 2839–2856. 10.1093/jxb/erv089 PubMed DOI
Xing C., Liu Y., Zhao L., Zhang S., Huang X. (2019). A novel MYB transcription factor regulates ascorbic acid synthesis and affects cold tolerance. Plant Cell Environ. 42, 832–845. 10.1111/pce.13387 PubMed DOI
Xing Y., Cao Q., Zhang Q., Qin L., Jia W., Zhang J. (2013). MKK5 regulates high light-induced gene expression of Cu/Zn superoxide dismutase 1 and 2 in Arabidopsis. Plant Cell Physiol. 54, 1217–1227. 10.1093/pcp/pct072 PubMed DOI
Xing Y., Chen W. H., Jia W., Zhang J. (2015). Mitogen-activated protein kinase kinase 5 (MKK5)-mediated signalling cascade regulates expression of iron superoxide dismutase gene in Arabidopsis under salinity stress. J. Exp. Bot. 66, 5971–5981. 10.1093/jxb/erv305 PubMed DOI PMC
Xing Y., Jia W., Zhang J. (2007). AtMEK1 mediates stress-induced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis. J. Exp. Bot. 58, 2969–2981. 10.1093/jxb/erm144 PubMed DOI
Xing Y., Jia W., Zhang J. (2008). AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J. 54, 440–451. 10.1111/j.1365-313X.2008.03433.x PubMed DOI
Xu J., Tran T., Padilla Marcia C. S., Braun D. M., Goggin F. L. (2017). Superoxide-responsive gene expression in Arabidopsis thaliana and Zea mays. Plant Physiol. Biochem. 117, 51–60. 10.1016/j.plaphy.2017.05.018 PubMed DOI
Xu P., Chen H., Cai W. (2020). Transcription factor CDF4 promotes leaf senescence and floral organ abscission by regulating abscisic acid and reactive oxygen species pathways in Arabidopsis. EMBO Rep. 21:e48967. 10.15252/embr.201948967 PubMed DOI PMC
Xue L., Wang P., Wang L., Renzi E., Radivojac P., Tang H., et al. . (2013). Quantitative measurement of phosphoproteome response to osmotic stress in Arabidopsis based on Library-Assisted eXtracted Ion Chromatogram (LAXIC). Mol. Cell. Proteomics 12, 2354–2369. 10.1074/mcp.O113.027284 PubMed DOI PMC
Xue Y., Zhou F., Zhu M., Ahmed K., Chen G., Yao X. (2005). GPS: a comprehensive www server for phosphorylation sites prediction. Nucleic Acids Res. 33, W184–W187. 10.1093/nar/gki393 PubMed DOI PMC
Yalcinkaya T., Uzilday B., Ozgur R., Turkan I., Mano J. (2019). Lipid peroxidation-derived reactive carbonyl species (RCS): their interaction with ROS and cellular redox during environmental stresses. Environ. Exp. Bot. 165, 139–149. 10.1016/j.envexpbot.2019.06.004 DOI
Yamasaki H., Abdel-Ghany S. E., Cohu C. M., Kobayashi Y., Shikanai T., Pilon M. (2007). Regulation of copper homeostasis by micro-RNA in Arabidopsis. J. Biol. Chem. 282, 16369–16378. 10.1074/jbc.M700138200 PubMed DOI
Yamasaki H., Hayashi M., Fukazawa M., Kobayashi Y., Shikanai T. (2009). SQUAMOSA promoter binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21, 347–361. 10.1105/tpc.108.060137 PubMed DOI PMC
Yan J., Guan L., Sun Y., Zhu Y., Liu L., Lu R., et al. . (2015). Calcium and ZmCCaMK are involved in brassinosteroid-induced antioxidant defense in maize leaves. Plant Cell Physiol. 56, 883–896. 10.1093/pcp/pcv014 PubMed DOI
Yang H., Mu J., Chen L., Feng J., Hu J., Li L., et al. . (2015). S-Nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol. 167, 1604–1615. 10.1104/pp.114.255216 PubMed DOI PMC
Yang Z., Guo G., Zhang M., Liu C. Y., Hu Q., Lam H., et al. . (2013). Stable isotope metabolic labeling-based quantitative phosphoproteomic analysis of Arabidopsis mutants reveals ethylene-regulated time-dependent phosphoproteins and putative substrates of constitutive triple response 1 kinase. Mol. Cell. Proteom. 12, 3559–3582. 10.1074/mcp.M113.031633 PubMed DOI PMC
Yang Z., Mhamdi A., Noctor G. (2019). Analysis of catalase mutants underscores the essential role of CATALASE2 for plant growth and day length-dependent oxidative signalling. Plant Cell Environ. 42, 688–700. 10.1111/pce.13453 PubMed DOI
Yin L., Mano J., Tanaka K., Wang S., Zhang M., Deng X., et al. . (2017). High level of reduced glutathione contributes to detoxification of lipid peroxide-derived reactive carbonyl species in transgenic Arabidopsis overexpressing glutathione reductase under aluminum stress. Physiol. Plant. 161, 211–223. 10.1111/ppl.12583 PubMed DOI
Yin L., Wang S., Eltayeb A. E., Uddin M. I., Yamamoto Y., Tsuji W., et al. . (2010). Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231, 609–621. 10.1007/s00425-009-1075-3 PubMed DOI
Yoshida K., Noguchi K., Motohashi K., Hisabori T. (2013). Systematic exploration of thioredoxin target proteins in plant mitochondria. Plant Cell Physiol. 54, 875–892. 10.1093/pcp/pct037 PubMed DOI
Yoshida S., Tamaoki M., Shikano T., Nakajima N., Ogawa D., Ioki M., et al. . (2006). Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana. Plant Cell Physiol. 47, 304–308. 10.1093/pcp/pci246 PubMed DOI
Yu X., Pasternak T., Eiblmeier M., Ditengou F., Kochersperger P., Sun J., et al. . (2013). Plastid-localized glutathione reductase2-regulated glutathione redox status is essential for Arabidopsis root apical meristem maintenance. Plant Cell 25, 4451–4468. 10.1105/tpc.113.11702 PubMed DOI PMC
Zandalinas S. I., Fichman Y., Devireddy A. R., Sengupta S., Azad R. K., Mittler R. (2020). Systemic signaling during abiotic stress combination in plants. Proc. Natl. Acad. Sci. U.S.A. 117, 13810–13820. 10.1073/pnas.2005077117 PubMed DOI PMC
Zandalinas S. I., Sengupta S., Burks D., Azad R. K., Mittler R. (2019). Identification and characterization of a core set of ROS wave-associated transcripts involved in the systemic acquired acclimation response of Arabidopsis to excess light. Plant J. 98, 126–141. 10.1111/tpj.14205 PubMed DOI PMC
Zechmann B. (2018). Compartment-specific importance of ascorbate during environmental stress in plants. Antioxid. Redox Signal. 29, 1488–1501. 10.1089/ars.2017.7232 PubMed DOI
Zhang A., Zhang J., Ye N., Cao J., Tan M., Zhang J., et al. . (2010). ZmMPK5 is required for the NADPH oxidase-mediated self-propagation of apoplastic H2O2 in brassinosteroid-induced antioxidant defence in leaves of maize. J. Exp. Bot. 61, 4399–4411. 10.1093/jxb/erq243 PubMed DOI PMC
Zhang H., Liu Y., Wen F., Yao D., Wang L., Guo J., et al. . (2014). A novel rice C2H2-type zinc finger protein, ZFP36, is a key player involved in abscisic acid-induced antioxidant defence and oxidative stress tolerance in rice. J. Exp. Bot. 65, 5795–5809. 10.1093/jxb/eru313 PubMed DOI PMC
Zhang H., Zhang Y., Deng C., Deng S., Li N., Zhao C., et al. . (2018). The Arabidopsis Ca2+-dependent protein kinase CPK12 is involved in plant response to salt stress. Int. J. Mol. Sci. 19:4062. 10.3390/ijms19124062 PubMed DOI PMC
Zhang H., Zhou H., Berke L., Heck A. J., Mohammed S., Scheres B., et al. . (2013). Quantitative phosphoproteomics after auxin-stimulated lateral root induction identifies an SNX1 protein phosphorylation site required for growth. Mol. Cell. Proteomics 12, 1158–1169. 10.1074/mcp.M112.021220 PubMed DOI PMC
Zhang M., Li Q., Liu T., Liu L., Shen D., Zhu Y., et al. . (2015). Two cytoplasmic effectors of Phytophthora sojae regulate plant cell death via interactions with plant catalases. Plant Physiol. 167, 164–175. 10.1104/pp.114.252437 PubMed DOI PMC
Zhang P., Wang R., Ju Q., Li W., Tran L. P., Xu J. (2019). The R2R3-MYB transcription factor MYB49 regulates cadmium accumulation. Plant Physiol. 180, 529–542. 10.1104/pp.18.01380 PubMed DOI PMC
Zhang P., Wang R., Yang X., Ju Q., Li W., Lü S., et al. . (2020). The R2R3-MYB transcription factor AtMYB49 modulates salt tolerance in Arabidopsis by modulating the cuticle formation and antioxidant defence. Plant Cell Environ. 43, 1925–1943. 10.1111/pce.13784 PubMed DOI
Zhang S., Li C., Ren H., Zhao T., Li Q., Wang S., et al. . (2020). BAK1 mediates light intensity to phosphorylate and activate catalases to regulate plant growth and development. Int. J. Mol. Sci. 21:1437. 10.3390/ijms21041437 PubMed DOI PMC
Zhang T., Zhu M., Song W. Y., Harmon A. C., Chen S. (2015). Oxidation and phosphorylation of MAP kinase 4 cause protein aggregation. Biochim. Biophys. Acta 1854, 156–165. 10.1016/j.bbapap.2014.11.006 PubMed DOI
Zhang Y., Ji T. T., Li T. T., Tian Y. Y., Wang L. F., Liu W. C. (2020). Jasmonic acid promotes leaf senescence through MYC2-mediated repression of CATALASE2 expression in Arabidopsis. Plant Sci. 299:110604. 10.1016/j.plantsci.2020.110604 PubMed DOI
Zhang Z., Wu Y., Gao M., Zhang J., Kong Q., Liu Y., et al. . (2012). Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11, 253–263. 10.1016/j.chom.2012.01.015 PubMed DOI
Zhao R., Sun H., Zhao N., Jing X., Shen X., Chen S. (2015). The Arabidopsis Ca2+-dependent protein kinase CPK27 is required for plant response to salt-stress. Gene 563, 203–214. 10.1016/j.gene.2015.03.024 PubMed DOI
Zhou Y. B., Liu C., Tang D. Y., Yan L., Wang D., Yang Y. Z., et al. . (2018). The receptor-like cytoplasmic kinase STRK1 phosphorylates and activates CatC, thereby regulating H2O2 homeostasis and improving salt tolerance in rice. Plant Cell 30, 1100–1118. 10.1105/tpc.17.01000 PubMed DOI PMC
Zimmermann P., Heinlein C., Orendi G., Zentgraf U. (2006). Senescence-specific regulation of catalases in Arabidopsis thaliana (L.) Heynh. Plant Cell Environ. 29, 1049–1060. 10.1111/j.1365-3040.2005.01459.x PubMed DOI
Zou J.-J., Li X.-D., Ratnasekera D., Wang C., Liu W.-X., Song L.-F., et al. . (2015). Arabidopsis CALCIUM-DEPENDENT PROTEIN KINASE8 and CATALASE3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress. Plant Cell 27, 1445–1460. 10.1105/tpc.15.00144 PubMed DOI PMC
Zulawski M., Braginets R., Schulze W. X. (2013). PhosPhAt goes kinases-searchable protein kinase target information in the plant phosphorylation site database PhosPhAt. Nucleic Acids Res. 41, D1176–D1184. 10.1093/nar/gks1081 PubMed DOI PMC
Zwack P. J., De Clercq I., Howton T. C., Hallmark H. T., Hurny A., Keshishian E. A., et al. . (2016). Cytokinin response factor 6 represses cytokinin-associated genes during oxidative stress. Plant Physiol. 172, 1249–1258. 10.1104/pp.16.00415 PubMed DOI PMC
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