Iron superoxide dismutase 1 (FSD1) was recently characterized as a plastidial, cytoplasmic, and nuclear enzyme with osmoprotective and antioxidant functions. However, the current knowledge on its role in oxidative stress tolerance is ambiguous. Here, we characterized the role of FSD1 in response to methyl viologen (MV)-induced oxidative stress in Arabidopsis thaliana. In accordance with the known regulation of FSD1 expression, abundance, and activity, the findings demonstrated that the antioxidant function of FSD1 depends on the availability of Cu2+ in growth media. Arabidopsis fsd1 mutants showed lower capacity to decompose superoxide at low Cu2+ concentrations in the medium. Prolonged exposure to MV led to reduced ascorbate levels and higher protein carbonylation in fsd1 mutants and transgenic plants lacking a plastid FSD1 pool as compared to the wild type. MV induced a rapid increase in FSD1 activity, followed by a decrease after 4 h long exposure. Genetic disruption of FSD1 negatively affected the hydrogen peroxide-decomposing ascorbate peroxidase in fsd1 mutants. Chloroplastic localization of FSD1 is crucial to maintain redox homeostasis. Proteomic analysis showed that the sensitivity of fsd1 mutants to MV coincided with decreased abundances of ferredoxin and photosystem II light-harvesting complex proteins. These mutants have higher levels of chloroplastic proteases indicating an altered protein turnover in chloroplasts. Moreover, FSD1 disruption affects the abundance of proteins involved in the defense response. Collectively, the study provides evidence for the conditional antioxidative function of FSD1 and its possible role in signaling.

Department of Biotechnology Faculty of Science Palacký University Olomouc Olomouc Czechia

Institute of Plant Physiology Russian Academy of Sciences Moscow Russia

Organismal and Evolutionary Biology Research Programme Faculty of Biological and Environmental Sciences Viikki Plant Science Centre University of Helsinki Helsinki Finland

Production Systems Unit Natural Resources Institute Finland Piikkiö Finland

Zobrazit více v PubMed

Amako K., Chen G.-X., Asada K. (1994). Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants. Plant Cell Physiol. 35 497–504. 10.1093/oxfordjournals.pcp.a078621 DOI

Babbs C. F., Pham J. A., Coolbaugh R. C. (1989). Lethal hydroxyl radical production in paraquat-treated plants. Plant Physiol. 90 1267–1270. 10.1104/pp.90.4.1267 PubMed DOI PMC

Bechtold U., Karpinski S., Mullineaux P. M. (2005). The influence of the light environment and photosynthesis on oxidative signalling responses in plant-biotrophic pathogen interactions. Plant Cell Environ. 28 1046–1055. 10.1111/j.1365-3040.2005.01340.x DOI

Benov L. (2001). How superoxide radical damages the cell. Protoplasma 217 33–36. 10.1007/BF01289410 PubMed DOI

Bradford M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 248–254. 10.1006/abio.1976.9999 PubMed DOI

Burkhead J. L., Gogolin Reynolds K. A., Abdel-Ghany S. E., Cohu C. M., Pilon M. (2009). Copper homeostasis. New Phytol. 182 799–816. 10.1111/j.1469-8137.2009.02846.x PubMed DOI

Camba R., Armstrong F. A. (2000). Investigations of the oxidative disassembly of Fe-S clusters in Clostridium pasteurianum 8Fe ferredoxin using pulsed-protein-film voltammetry. Biochemistry 39 10587–10598. 10.1021/bi000832+ PubMed DOI

Chen S., Dickman M. B. (2004). Bcl-2 family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides. J. Exp. Bot. 55 2617–2623. 10.1093/jxb/erh275 PubMed DOI

Chia L. S., McRae D. G., Thompson J. E. (1982). Light-dependence of paraquat-initiated membrane deterioration in bean plants. Evidence for the involvement of superoxide. Physiol. Plant 56 492–499. 10.1111/j.1399-3054.1982.tb04545.x DOI

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

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. (2021a). 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

Dvořák P., Krasylenko Y., Zeiner A., Šamaj J., Takáč T. (2021b). Signaling toward reactive oxygen species-scavenging enzymes in plants. Front. Plant Sci. 11:618835. 10.3389/fpls.2020.618835 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

Farrington J. A., Ebert M., Land E. J., Fletcher K. (1973). Bipyridylium quaternary salts and related compounds. V. Pulse radiolysis studies of the reaction of paraquat radical with oxygen. Implications for the mode of action of bipyridyl herbicides. Biochim. Biophys. Acta 314 372–381. 10.1016/0005-2728(73)90121-7 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. (2005). Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ. 28 1056–1071. 10.1111/j.1365-3040.2005.01327.x DOI

Frese C. K., van den Toorn H., Heck A. J. R., Mohammed S. (2019). “Quantitative proteomics for differential protein expression profiling,” in Proteomics for Biological Discovery, eds Veenstra T. D., Yates J. R. (Hoboken, NJ: John Wiley & Sons, Inc.), 1–27. 10.1002/9781119081661.ch1 DOI

Fridovich I. (1978). Superoxide radicals, superoxide dismutases and the aerobic lifestyle. Photochem. Photobiol. 28 733–741. 10.1111/j.1751-1097.1978.tb07009.x PubMed DOI

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

Gillespie K. M., Ainsworth E. A. (2007). Measurement of reduced, oxidized and total ascorbate content in plants. Nat. Protoc. 2 871–874. 10.1038/nprot.2007.101 PubMed DOI

Han H.-J., Peng R.-H., Zhu B., Fu X.-Y., Zhao W., Shi B., et al. (2014). Gene expression profiles of Arabidopsis under the stress of methyl viologen: a microarray analysis. Mol. Biol. Rep. 41 7089–7102. 10.1007/s11033-014-3396-y PubMed DOI

Hanke G., Mulo P. (2013). Plant type ferredoxins and ferredoxin-dependent metabolism: chloroplast ferredoxins. Plant Cell Environ. 36 1071–1084. 10.1111/pce.12046 PubMed DOI

Hanke G. T., Hase T. (2008). Variable photosynthetic roles of two leaf-type ferredoxins in Arabidopsis, as revealed by RNA interference. Photochem. Photobiol. 84 1302–1309. 10.1111/j.1751-1097.2008.00411.x PubMed DOI

Hawkes T. R. (2014). Mechanisms of resistance to paraquat in plants. Pest Manag. Sci. 70 1316–1323. 10.1002/ps.3699 PubMed DOI

Hossain M. S., Dietz K.-J. (2016). Tuning of redox regulatory mechanisms, reactive oxygen species and redox homeostasis under salinity stress. Front. Plant Sci. 7:548. 10.3389/fpls.2016.00548 PubMed DOI PMC

Hubert D. A., He Y., McNulty B. C., Tornero P., Dangl J. L. (2009). Specific Arabidopsis HSP90.2 alleles recapitulate RAR1 cochaperone function in plant NB-LRR disease resistance protein regulation. Proc. Natl. Acad. Sci. U.S.A. 106 9556–9563. 10.1073/pnas.0904877106 PubMed DOI PMC

Imlay J. A. (2003). Pathways of oxidative damage. Annu. Rev. Microbiol. 57 395–418. 10.1146/annurev.micro.57.030502.090938 PubMed DOI

Imlay J. A. (2006). Iron-sulphur clusters and the problem with oxygen. Mol. Microbiol. 59 1073–1082. 10.1111/j.1365-2958.2006.05028.x PubMed DOI

Imlay J. A. (2008). Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 77 755–776. 10.1146/annurev.biochem.77.061606.161055 PubMed DOI PMC

Iriel A., Novo J. M., Cordon G. B., Lagorio M. G. (2014). Atrazine and methyl viologen effects on chlorophyll-a fluorescence revisited-Implications in photosystems emission and ecotoxicity assessment. Photochem. Photobiol. 90 107–112. 10.1111/php.12142 PubMed DOI

Ivanov B. N., Borisova-Mubarakshina M. M., Kozuleva M. A. (2018). Formation mechanisms of superoxide radical and hydrogen peroxide in chloroplasts, and factors determining the signalling by hydrogen peroxide. Funct. Plant Biol. 45 102–110. 10.1071/FP16322 PubMed DOI

Kameoka T., Okayasu T., Kikuraku K., Ogawa T., Sawa Y., Yamamoto H., et al. (2021). Cooperation of chloroplast ascorbate peroxidases and proton gradient regulation 5 is critical for protecting Arabidopsis plants from photo-oxidative stress. Plant J. 107 876–892. 10.1111/tpj.15352 PubMed DOI

Kato Y., Sakamoto W. (2009). Protein quality control in chloroplasts: a current model of D1 protein degradation in the photosystem II repair cycle. J. Biochem. 146 463–469. 10.1093/jb/mvp073 PubMed DOI

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

Kozuleva M. A., Ivanov B. N. (2016). The Mechanisms of oxygen reduction in the terminal reducing segment of the chloroplast photosynthetic electron transport chain. Plant Cell Physiol. 57 1397–1404. 10.1093/pcp/pcw035 PubMed DOI

Krieger-Liszkay A., Kós P. B., Hideg E. (2011). Superoxide anion radicals generated by methylviologen in photosystem I damage photosystem II. Physiol. Plant 142 17–25. 10.1111/j.1399-3054.2010.01416.x PubMed DOI

Krynická V., Shao S., Nixon P. J., Komenda J. (2015). Accessibility controls selective degradation of photosystem II subunits by FtsH protease. Nat. Plants 1 1–6. 10.1038/nplants.2015.168 PubMed DOI

Lennicke C., Rahn J., Heimer N., Lichtenfels R., Wessjohann L. A., Seliger B. (2016). Redox proteomics: methods for the identification and enrichment of redox-modified proteins and their applications. Proteomics 16 197–213. 10.1002/pmic.201500268 PubMed DOI

Li F., Wu Q.-Y., Sun Y.-L., Wang L.-Y., Yang X.-H., Meng Q.-W. (2010). Overexpression of chloroplastic monodehydroascorbate reductase enhanced tolerance to temperature and methyl viologen-mediated oxidative stresses. Physiol. Plant 139 421–434. 10.1111/j.1399-3054.2010.01369.x PubMed DOI

Liu J., Wang P., Liu B., Feng D., Zhang J., Su J., et al. (2013). A deficiency in chloroplastic ferredoxin 2 facilitates effective photosynthetic capacity during long-term high light acclimation in Arabidopsis thaliana. Plant J. 76 861–874. 10.1111/tpj.12341 PubMed DOI

Malnoë A., Wang F., Girard-Bascou J., Wollman F.-A., de Vitry C. (2014). Thylakoid FtsH protease contributes to photosystem II and cytochrome b6f remodeling in Chlamydomonas reinhardtii under stress conditions. Plant Cell 26 373–390. 10.1105/tpc.113.120113 PubMed DOI PMC

McCord J. M., Keele B. B., Fridovich I. (1971). An enzyme-based theory of obligate anaerobiosis: the physiological function of superoxide dismutase. Proc. Natl. Acad. Sci. U.S.A. 68 1024–1027. 10.1073/pnas.68.5.1024 PubMed DOI PMC

Mermod M., Takusagawa M., Kurata T., Kamiya T., Fujiwara T., Shikanai T. (2019). SQUAMOSA promoter-binding protein-like 7 mediates copper deficiency response in the presence of high nitrogen in Arabidopsis thaliana. Plant Cell Rep. 38 835–846. 10.1007/s00299-019-02422-0 PubMed DOI

Mock H.-P., Dietz K.-J. (2016). Redox proteomics for the assessment of redox-related posttranslational regulation in plants. Biochim. Biophys. Acta (BBA) - Proteins Proteomics 1864 967–973. 10.1016/j.bbapap.2016.01.005 PubMed DOI

Morgan M. J., Lehmann M., Schwarzländer M., Baxter C. J., Sienkiewicz-Porzucek A., Williams T. C. R., 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

Murashige T., Skoog F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant 15 473–497. 10.1111/j.1399-3054.1962.tb08052.x DOI

Muthuramalingam M., Matros A., Scheibe R., Mock H.-P., Dietz K.-J. (2013). The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo. Front. Plant Sci. 4:54. 10.3389/fpls.2013.00054 PubMed DOI PMC

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

Nelson C. J., Alexova R., Jacoby R. P., Millar A. H. (2014). Proteins with high turnover rate in barley leaves estimated by proteome analysis combined with in planta isotope labeling. Plant Physiol. 166 91–108. 10.1104/pp.114.243014 PubMed DOI PMC

Nishiyama Y., Allakhverdiev S. I., Murata N. (2006). A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim. Biophys. Acta 1757 742–749. 10.1016/j.bbabio.2006.05.013 PubMed DOI

Nishiyama Y., Yamamoto H., Allakhverdiev S. I., Inaba M., Yokota A., Murata N. (2001). Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J. 20 5587–5594. 10.1093/emboj/20.20.5587 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

Perez-Riverol Y., Csordas A., Bai J., Bernal-Llinares M., Hewapathirana S., Kundu D. J., et al. (2019). The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 47 D442–D450. 10.1093/nar/gky1106 PubMed DOI PMC

Pilon M., Ravet K., Tapken W. (2011). The biogenesis and physiological function of chloroplast superoxide dismutases. Biochim. Biophys. Acta (BBA) - Bioenerget. 1807 989–998. 10.1016/j.bbabio.2010.11.002 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

Rantala M., Rantala S., Aro E.-M. (2020). Composition, phosphorylation and dynamic organization of photosynthetic protein complexes in plant thylakoid membrane. Photochem. Photobiol. Sci. 19 604–619. 10.1039/D0PP00025F PubMed DOI

Ravet K., Touraine B., Boucherez J., Briat J.-F., Gaymard F., Cellier F. (2009). Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J. 57 400–412. 10.1111/j.1365-313X.2008.03698.x PubMed DOI

Reif D. W. (1992). Ferritin as a source of iron for oxidative damage. Free Radic. Biol. Med. 12 417–427. 10.1016/0891-5849(92)90091-t PubMed DOI

Scarpeci T. E., Zanor M. I., Carrillo N., Mueller-Roeber B., Valle E. M. (2008). Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes. Plant Mol. Biol. 66 361–378. 10.1007/s11103-007-9274-4 PubMed DOI PMC

Schneider C. A., Rasband W. S., Eliceiri K. W. (2012). NIH Image to ImageJ:25 years of image analysis. Nat. Methods 9 671–675. 10.1038/nmeth.2089 PubMed DOI PMC

Sewelam N., Jaspert N., Van Der Kelen K., Tognetti V. B., Schmitz J., Frerigmann H., et al. (2014). Spatial H2O2 signaling specificity: H2O2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially. Mol. Plant 7 1191–1210. 10.1093/mp/ssu070 PubMed 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

Song Y. G., Liu B., Wang L. F., Li M. H., Liu Y. (2006). Damage to the oxygen-evolving complex by superoxide anion, hydrogen peroxide, and hydroxyl radical in photoinhibition of photosystem II. Photosynth Res. 90 67–78. 10.1007/s11120-006-9111-7 PubMed DOI

Suntres Z. E. (2002). Role of antioxidants in paraquat toxicity. Toxicology 180 65–77. 10.1016/s0300-483x(02)00382-7 PubMed DOI

Takáč T., Pechan T., Šamaj J. (2011). Differential proteomics of plant development. J. Proteomics 74 577–588. 10.1016/j.jprot.2011.02.002 PubMed DOI

Takáč T., Šamajová O., Pechan T., Luptovčiak I., Šamaj J. (2017). Feedback microtubule control and microtubule-actin cross-talk in Arabidopsis revealed by integrative proteomic and cell biology analysis of KATANIN 1 mutants. Mol. Cell Prot. 16 1591–1609. 10.1074/mcp.M117.068015 PubMed DOI PMC

Takáč T., Šamajová O., Vadovič P., Pechan T., Košútová P., Ovečka M., et al. (2014). Proteomic and biochemical analyses show functional network of proteins involved in antioxidant defense of Arabidopsis anp2anp3 double mutant. J. Prot. Res. 13 5347–5361. 10.1021/pr500588c PubMed DOI PMC

Takahashi M., Asada K. (1988). Superoxide production in aprotic interior of chloroplast thylakoids. Arch. Biochem. Biophys. 267 714–722. 10.1016/0003-9861(88)90080-x PubMed DOI

Toruño T. Y., Shen M., Coaker G., Mackey D. (2019). Regulated disorder: posttranslational modifications control the RIN4 plant immune signaling hub. Mol. Plant Microbe Interact. 32 56–64. 10.1094/MPMI-07-18-0212-FI PubMed DOI PMC

Tsang C. K., Liu Y., Thomas J., Zhang Y., Zheng X. F. S. (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

Valasatava Y., Rosato A., Banci L., Andreini C. (2016). MetalPredator: a web server to predict iron–sulfur cluster binding proteomes. Bioinformatics 32 2850–2852. 10.1093/bioinformatics/btw238 PubMed DOI

Van Breusegem F., Slooten L., Stassart J. M., Moens T., Botterman J., Van Montagu M., et al. (1999). Overproduction of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize. Plant Cell Physiol. 40 515–523. 10.1093/oxfordjournals.pcp.a029572 PubMed DOI

Van Camp W., Capiau K., Van Montagu M., Inzé D., Slooten L. (1996). Enhancement of oxidative stress tolerance in transgenic tobacco plants overproducing Fe-superoxide dismutase in chloroplasts. Plant Physiol. 112 1703–1714. 10.1104/pp.112.4.1703 PubMed DOI PMC

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

Waters B. M., McInturf S. A., Stein R. J. (2012). Rosette iron deficiency transcript and microRNA profiling reveals links between copper and iron homeostasis in Arabidopsis thaliana. J. Exp. Bot. 63 5903–5918. 10.1093/jxb/ers239 PubMed DOI PMC

Wong P. K. (2000). Effects of 2,4-D, glyphosate and paraquat on growth, photosynthesis and chlorophyll-a synthesis of Scenedesmus quadricauda Berb 614. Chemosphere 41 177–182. 10.1016/s0045-6535(99)00408-7 PubMed DOI

Xiong Y., Contento A. L., Nguyen P. Q., Bassham D. C. (2007). Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol. 143 291–299. 10.1104/pp.106.092106 PubMed DOI PMC

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

Zhang J., Vancea A. I., Shahul Hameed U. F., Arold S. T. (2021). Versatile control of the CDC48 segregase by the plant UBX-containing (PUX) proteins. Comput. Struct. Biotechnol. J. 19 3125–3132. 10.1016/j.csbj.2021.05.025 PubMed DOI PMC

Methyl viologen-induced changes in the Arabidopsis proteome implicate PATELLIN 4 in oxidative stress responses

Protein-protein interactions in plant antioxidant defense