{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,11]],"date-time":"2026-02-11T18:51:53Z","timestamp":1770835913387,"version":"3.50.1"},"reference-count":92,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2023,6,4]],"date-time":"2023-06-04T00:00:00Z","timestamp":1685836800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada (NSERC)","doi-asserted-by":"publisher","award":["DGECR-2019-00304"],"award-info":[{"award-number":["DGECR-2019-00304"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Protein carbonylation is an irreversible form of post-translational modification triggered by reactive oxygen species in animal and plant cells. It occurs either through the metal-catalyzed oxidation of Lys, Arg, Pro, and Thr side chains or the addition of \u03b1, \u03b2-unsaturated aldehydes and ketones to the side chains of Cys, Lys, and His. Recent genetic studies concerning plants pointed to an implication of protein carbonylation in gene regulation through phytohormones. However, for protein carbonylation to stand out as a signal transduction mechanism, such as phosphorylation and ubiquitination, it must be controlled in time and space by a still unknown trigger. In this study, we tested the hypothesis that the profile and extent of protein carbonylation are influenced by iron homeostasis in vivo. For this, we compared the profile and the contents of the carbonylated proteins in the Arabidopsis thaliana wild-type and mutant-deficient in three ferritin genes under normal and stress conditions. Additionally, we examined the proteins specifically carbonylated in wild-type seedlings exposed to iron-deficient conditions. Our results indicated that proteins were differentially carbonylated between the wild type and the triple ferritin mutant Fer1-3-4 in the leaves, stems, and flowers under normal growth conditions. The profile of the carbonylated proteins was also different between the wild type and the ferritin triple mutant exposed to heat stress, thus pointing to the influence of iron on the carbonylation of proteins. Consistent with this, the exposure of the seedlings to iron deficiency and iron excess greatly influenced the carbonylation of certain proteins involved in intracellular signal transduction, translation, and iron deficiency response. Overall, the study underlined the importance of iron homeostasis in the occurrence of protein carbonylation in vivo.<\/jats:p>","DOI":"10.3390\/ijms24119732","type":"journal-article","created":{"date-parts":[[2023,6,5]],"date-time":"2023-06-05T04:01:47Z","timestamp":1685937707000},"page":"9732","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Iron Availability Influences Protein Carbonylation in Arabidopsis thaliana Plants"],"prefix":"10.3390","volume":"24","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0599-6559","authenticated-orcid":false,"given":"Adesola J.","family":"Tola","sequence":"first","affiliation":[{"name":"Groupe de Recherche en Biologie V\u00e9g\u00e9tale (GRBV), Department of Chemistry, Biochemistry and Physics, Universit\u00e9 du Qu\u00e9bec \u00e0 Trois-Rivi\u00e8res, 3351 Boul. des Forges, Trois-Rivi\u00e8res, QC G9A 5H7, Canada"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5905-2970","authenticated-orcid":false,"given":"Tagnon D.","family":"Missihoun","sequence":"additional","affiliation":[{"name":"Groupe de Recherche en Biologie V\u00e9g\u00e9tale (GRBV), Department of Chemistry, Biochemistry and Physics, Universit\u00e9 du Qu\u00e9bec \u00e0 Trois-Rivi\u00e8res, 3351 Boul. des Forges, Trois-Rivi\u00e8res, QC G9A 5H7, Canada"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,6,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"3766","DOI":"10.1021\/pr1002609","article-title":"Proteomic Identification of Carbonylated Proteins and Their Oxidation Sites","volume":"9","author":"Madian","year":"2010","journal-title":"J. Proteome Res."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Tola, A.J., Jaballi, A., and Missihoun, T.D. (2021). Protein Carbonylation: Emerging Roles in Plant Redox Biology and Future Prospects. Plants, 10.","DOI":"10.3390\/plants10071451"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"862","DOI":"10.3390\/biom4030862","article-title":"Regulating the 20S Proteasome Ubiquitin-Independent Degradation Pathway","volume":"4","author":"Sharon","year":"2014","journal-title":"Biomolecules"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/j.molcel.2017.12.021","article-title":"Maintaining a Healthy Proteome during Oxidative Stress","volume":"69","author":"Reichmann","year":"2018","journal-title":"Mol. Cell"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1111\/j.1582-4934.2006.tb00407.x","article-title":"Protein carbonylation, cellular dysfunction, and disease progression","volume":"10","author":"Aldini","year":"2006","journal-title":"J. Cell. Mol. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2228","DOI":"10.1016\/j.jprot.2011.05.004","article-title":"Protein carbonylation and metal-catalyzed protein oxidation in a cellular perspective","volume":"74","author":"Rao","year":"2011","journal-title":"J. Proteom."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1104\/pp.115.256834","article-title":"Lipid Peroxide-Derived Short-Chain Carbonyls Mediate Hydrogen Peroxide-Induced and Salt-Induced Programmed Cell Death in Plants","volume":"168","author":"Biswas","year":"2015","journal-title":"Plant Physiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2552","DOI":"10.1093\/pcp\/pcw166","article-title":"Reactive Carbonyl Species Mediate ABA Signaling in Guard Cells","volume":"57","author":"Islam","year":"2016","journal-title":"Plant Cell Physiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"536","DOI":"10.1111\/tpj.14456","article-title":"Reactive oxygen species and reactive carbonyl species constitute a feed-forward loop in auxin signaling for lateral root formation","volume":"100","author":"Biswas","year":"2019","journal-title":"Plant J."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1146\/annurev.arplant.58.032806.103946","article-title":"Oxidative Modifications to Cellular Components in Plants","volume":"58","author":"Jensen","year":"2007","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1016\/j.tplants.2010.04.008","article-title":"ROS signalling\u2014specificity is required","volume":"15","author":"Sweetlove","year":"2010","journal-title":"Trends Plant Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"e13658","DOI":"10.1111\/ppl.13658","article-title":"The phytohormone abscisic acid modulates protein carbonylation in Arabidopsis thaliana","volume":"174","author":"Jaballi","year":"2022","journal-title":"Physiol. Plant."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1839","DOI":"10.1016\/j.phytochem.2004.04.007","article-title":"Identification of oxidised proteins in the matrix of rice leaf mitochondria by immunoprecipitation and two-dimensional liquid chromatography-tandem mass spectrometry","volume":"65","author":"Kristensen","year":"2004","journal-title":"Phytochemistry"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0065-2296(10)52001-9","article-title":"Chapter 1 Oxidation of Proteins in Plants\u2014Mechanisms and Consequences","volume":"52","author":"Sweetlove","year":"2009","journal-title":"Adv. Bot. Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"5081","DOI":"10.1039\/c3an00724c","article-title":"Qualitative and quantitative evaluation of derivatization reagents for different types of protein-bound carbonyl groups","volume":"138","author":"Bollineni","year":"2013","journal-title":"Analyst"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/S0300-483X(00)00231-6","article-title":"The Haber-Weiss reaction and mechanisms of toxicity","volume":"149","author":"Kehrer","year":"2000","journal-title":"Toxicology"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"35749","DOI":"10.1074\/jbc.M706838200","article-title":"Genetic Removal of Tri-unsaturated Fatty Acids Suppresses Developmental and Molecular Phenotypes of an Arabidopsis Tocopherol-deficient Mutant: Whole-Body Mapping of Malondialdehyde Pools in a Complex Eukaryote","volume":"282","author":"Davoine","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"969","DOI":"10.1016\/0378-4274(95)03532-X","article-title":"Toxicity of iron and hydrogen peroxide: The Fenton reaction","volume":"82\u201383","author":"Winterbourn","year":"1995","journal-title":"Toxicol. Lett."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1016\/j.tplants.2009.02.006","article-title":"Homing in on iron homeostasis in plants","volume":"14","author":"Jeong","year":"2009","journal-title":"Trends Plant Sci."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Broadley, M., Brown, P., Cakmak, I., Rengel, Z., and Zhao, F. (2012). Function of Nutrients. Marschner\u2019s Miner. Nutr. High. Plants Third Ed., 191\u2013248.","DOI":"10.1016\/B978-0-12-384905-2.00007-8"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1223","DOI":"10.1105\/tpc.001388","article-title":"IRT1, an arabidopsis transporter essential for iron uptake from the soil and for plant growth","volume":"14","author":"Vert","year":"2002","journal-title":"Plant Cell"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"350","DOI":"10.3389\/fpls.2013.00350","article-title":"New insights into Fe localization in plant tissues","volume":"4","author":"Roschzttardtz","year":"2013","journal-title":"Front. Plant Sci."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Mahender, A., Swamy, B.P.M., Anandan, A., and Ali, J. (2019). Tolerance of Iron-Deficient and -Toxic Soil Conditions in Rice. Plants, 8.","DOI":"10.3390\/plants8020031"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1002\/jpln.200520504","article-title":"Iron toxicity in rice\u2014conditions and management concepts","volume":"168","author":"Becker","year":"2005","journal-title":"J. Plant Nutr. Soil Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1146\/annurev-arplant-042811-105522","article-title":"Iron Uptake, Translocation, and Regulation in Higher Plants","volume":"63","author":"Kobayashi","year":"2012","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"852","DOI":"10.1111\/pce.12203","article-title":"Abscisic acid alleviates iron deficiency by promoting root iron reutilization and transport from root to shoot in Arabidopsis","volume":"37","author":"Lei","year":"2014","journal-title":"Plant Cell Environ."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.1365-313X.2008.03502.x","article-title":"Cytokinins negatively regulate the root iron uptake machinery in Arabidopsis through a growth-dependent pathway","volume":"55","author":"Briat","year":"2008","journal-title":"Plant J."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1016\/j.plaphy.2011.01.025","article-title":"Suppression of Fe deficiency gene expression by jasmonate","volume":"49","author":"Maurer","year":"2011","journal-title":"Plant Physiol. Biochem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1016\/S1360-1385(02)02312-9","article-title":"Oxidative stress, antioxidants and stress tolerance","volume":"7","author":"Mittler","year":"2002","journal-title":"Trends Plant Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1007\/s001220050861","article-title":"Evolutionary relationship of plant catalase genes inferred from exon-intron structures: Isozyme divergence after the separation of monocots and dicots","volume":"97","author":"Iwamoto","year":"1998","journal-title":"Theor. Appl. Genet."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1011","DOI":"10.1590\/S1415-47572012000600016","article-title":"Plant responses to stresses: Role of ascorbate peroxidase in the antioxidant protection","volume":"35","author":"Caverzan","year":"2012","journal-title":"Genet. Mol. Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"764","DOI":"10.1016\/j.freeradbiomed.2022.11.019","article-title":"Plant thiol peroxidases as redox sensors and signal transducers in abiotic stress acclimation","volume":"193","author":"Vogelsang","year":"2022","journal-title":"Free. Radic. Biol. Med."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"K\u00f6nig, J., Jung, T., and Grune, T. (2017). Protein Carbonylation in Aging and Senescence. Protein Carbonylation Princ. Anal. Biol. Implic., 272\u2013290.","DOI":"10.1002\/9781119374947.ch11"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1007\/BF00026783","article-title":"Iron induces ferritin synthesis in maize plantlets","volume":"19","author":"Massenet","year":"1992","journal-title":"Plant Mol. Biol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1093\/aob\/mcp128","article-title":"New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants","volume":"105","author":"Briat","year":"2010","journal-title":"Ann. Bot."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"18148","DOI":"10.1016\/S0021-9258(19)37165-0","article-title":"Ferritin: A cytoprotective antioxidant strategem of endothelium","volume":"267","author":"Balla","year":"1992","journal-title":"J. Biol. Chem."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"3657","DOI":"10.1111\/j.1432-1033.2004.04300.x","article-title":"Evidence for the presence of ferritin in plant mitochondria","volume":"271","author":"Zancani","year":"2004","journal-title":"Eur. J. Biol. Chem."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1016\/j.jplph.2009.10.015","article-title":"Knocking out of the mitochondrial AtFer4 ferritin does not alter response of Arabidopsis plants to abiotic stresses","volume":"167","author":"Tarantino","year":"2010","journal-title":"J. Plant Physiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1146\/annurev.bi.56.070187.001445","article-title":"FERRITIN: STRUCTURE, GENE REGULATION, AND CELLULAR FUNCTION IN ANIMALS, PLANTS, AND MICROORGANISMS","volume":"56","author":"Theil","year":"1987","journal-title":"Annu. Rev. Biochem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/S1360-1385(97)85225-9","article-title":"Iron transport and storage in plants","volume":"2","author":"Briat","year":"1997","journal-title":"Trends Plant Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1146\/annurev.arplant.54.031902.135018","article-title":"Iron Transport and Signaling in Plants","volume":"54","author":"Curie","year":"2003","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/0005-2728(96)00022-9","article-title":"The ferritins: Molecular properties, iron storage function and cellular regulation","volume":"1275","author":"Harrison","year":"1996","journal-title":"Biochim. Biophys. Acta Bioenerg."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1007\/s00775-006-0125-6","article-title":"Ferritins: Iron\/oxygen biominerals in protein nanocages","volume":"11","author":"Theil","year":"2006","journal-title":"JBIC J. Biol. Inorg. Chem."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1042\/bj3180067","article-title":"Characterization of a ferritin mRNA from Arabidopsis thaliana accumulated in response to iron through an oxidative pathway independent of abscisic acid","volume":"318","author":"Gaymard","year":"1996","journal-title":"Biochem. J."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Yadav, K., Patel, P., Srivastava, A.K., and Ganapathi, T.R. (2017). Overexpression of native ferritin gene MusaFer1 enhances iron content and oxidative stress tolerance in transgenic banana plants. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0188933"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1042\/bj3590575","article-title":"Structure and differential expression of the four members of the Arabidopsis thaliana ferritin gene family","volume":"359","author":"Petit","year":"2001","journal-title":"Biochem. J."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1111\/j.1365-313X.2008.03698.x","article-title":"Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis","volume":"57","author":"Ravet","year":"2009","journal-title":"Plant J."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"730","DOI":"10.1021\/pr900538e","article-title":"Oxidative Stress Studies in Yeast with a Frataxin Mutant: A Proteomics Perspective","volume":"9","author":"Kim","year":"2010","journal-title":"J. Proteome Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1111\/j.1365-313X.2006.02923.x","article-title":"Deficiency of Arabidopsis thaliana frataxin alters activity of mitochondrial Fe-S proteins and induces oxidative stress","volume":"48","author":"Busi","year":"2006","journal-title":"Plant J."},{"key":"ref_50","first-page":"1499","article-title":"Growth Stage-Based Phenotypic Analysis of Arabidopsis: A Model for High Throughput Functional Genomics in Plants","volume":"13","author":"Boyes","year":"2001","journal-title":"Plant Cell"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1728","DOI":"10.1093\/plphys\/kiab329","article-title":"IRONMAN tunes responses to iron deficiency in concert with environmental pH","volume":"187","author":"Gautam","year":"2021","journal-title":"Plant Physiol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"e4324","DOI":"10.21769\/BioProtoc.4342","article-title":"A Quick Method to Quantify Iron in Arabidopsis Seedlings Iron Transport in Plants View Project PH Sensing in Plants View Project","volume":"12","author":"Gautam","year":"2022","journal-title":"Bio. Protoc."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1510","DOI":"10.1104\/pp.18.00533","article-title":"Protein Carbonylation and Glycation in Legume Nodules","volume":"177","author":"Matamoros","year":"2018","journal-title":"Plant Physiol."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Rojas Echeverri, J.C., Milkovska-Stamenova, S., and Hoffmann, R. (2021). A workflow towards the reproducible identification and quantitation of protein carbonylation sites in human plasma. Antioxidants, 10.","DOI":"10.3390\/antiox10030369"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"6847","DOI":"10.1021\/ac0607257","article-title":"New Role for an Old Probe: Affinity Labeling of Oxylipid Protein Conjugates by N\u2018-Aminooxymethylcarbonylhydrazino d-biotin","volume":"78","author":"Chavez","year":"2006","journal-title":"Anal. Chem."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/j.freeradbiomed.2013.11.030","article-title":"Proteome-wide profiling of carbonylated proteins and carbonylation sites in HeLa cells under mild oxidative stress conditions","volume":"68","author":"Bollineni","year":"2014","journal-title":"Free. Radic. Biol. Med."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1104\/pp.103.029066","article-title":"Environmentally Induced Plasticity of Root Hair Development in Arabidopsis","volume":"134","author":"Schmidt","year":"2004","journal-title":"Plant Physiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2697","DOI":"10.1093\/jxb\/erl035","article-title":"RACK1 mediates multiple hormone responsiveness and developmental processes in Arabidopsis","volume":"57","author":"Chen","year":"2006","journal-title":"J. Exp. Bot."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"3819","DOI":"10.1093\/jxb\/erp221","article-title":"RACK1 is a negative regulator of ABA responses in Arabidopsis","volume":"60","author":"Guo","year":"2009","journal-title":"J. Exp. Bot."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"2628","DOI":"10.1093\/bioinformatics\/btz931","article-title":"ShinyGO: A Graphical Gene-Set Enrichment Tool for Animals and Plants","volume":"36","author":"Ge","year":"2020","journal-title":"Bioinformatics"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"D1064","DOI":"10.1093\/nar\/gkw1041","article-title":"SUBA4: The interactive data analysis centre for Arabidopsis subcellular protein locations","volume":"45","author":"Hooper","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"22204","DOI":"10.1074\/jbc.M402652200","article-title":"Progression and Specificity of Protein Oxidation in the Life Cycle of Arabidopsis thaliana","volume":"279","author":"Johansson","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"257","DOI":"10.4161\/auto.3847","article-title":"Disruption of Autophagy Results in Constitutive Oxidative Stress in Arabidopsis","volume":"3","author":"Xiong","year":"2007","journal-title":"Autophagy"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/j.molp.2014.11.014","article-title":"Iron- and Ferritin-Dependent Reactive Oxygen Species Distribution: Impact on Arabidopsis Root System Architecture","volume":"8","author":"Reyt","year":"2015","journal-title":"Mol. Plant"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"806","DOI":"10.1016\/j.bbagen.2009.12.003","article-title":"Ferritins and iron storage in plants","volume":"1800","author":"Briat","year":"2010","journal-title":"Biochim. Biophys. Acta Gen. Subj."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1433","DOI":"10.1111\/nph.15753","article-title":"Transcriptional integration of the responses to iron availability in Arabidopsis by the bHLH factor ILR3","volume":"223","author":"Tissot","year":"2019","journal-title":"New Phytol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/S0176-1617(11)81418-5","article-title":"The Effects of Cadmium on the Fluidity and H+-ATPase Activity of Plasma Membrane from Sunflower and Wheat Roots","volume":"147","author":"Fodor","year":"1995","journal-title":"J. Plant Physiol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1007\/BF00958964","article-title":"Phosphorylation of the plasma-membrane H+-ATPase of oat roots by a calcium-stimulated protein kinase","volume":"173","author":"Schaller","year":"1988","journal-title":"Planta"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/S0304-4157(99)00011-8","article-title":"Regulation of plasma membrane H+-ATPase in fungi and plants","volume":"1469","author":"Portillo","year":"2000","journal-title":"Biochim. et Biophys. Acta (BBA) - Rev. Biomembr."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1186\/1471-2164-14-783","article-title":"Expression changes of ribosomal proteins in phosphate- and iron-deficient Arabidopsis roots predict stress-specific alterations in ribosome composition","volume":"14","author":"Wang","year":"2013","journal-title":"BMC Genom."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"e00230-18","DOI":"10.1128\/MCB.00230-18","article-title":"RACK1 Specifically Regulates Translation through Its Binding to Ribosomes","volume":"38","author":"Gallo","year":"2018","journal-title":"Mol. Cell. Biol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1104\/pp.110.160663","article-title":"Involvement of Arabidopsis RACK1 in Protein Translation and Its Regulation by Abscisic Acid","volume":"155","author":"Guo","year":"2011","journal-title":"Plant Physiol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1038\/s41598-019-57132-0","article-title":"Global translational repression induced by iron deficiency in yeast depends on the Gcn2\/eIF2\u03b1 pathway","volume":"10","author":"Romero","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"2219","DOI":"10.1105\/tpc.110.074096","article-title":"The bHLH Transcription Factor POPEYE Regulates Response to Iron Deficiency in Arabidopsis Roots","volume":"22","author":"Long","year":"2010","journal-title":"Plant Cell"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1104\/pp.114.250837","article-title":"Iron-Binding E3 Ligase Mediates Iron Response in Plants by Targeting Basic Helix-Loop-Helix Transcription Factors","volume":"167","author":"Selote","year":"2015","journal-title":"Plant Physiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"2463","DOI":"10.1111\/pce.13363","article-title":"The E3 ligase BRUTUS facilitates degradation of VOZ1\/2 transcription factors","volume":"41","author":"Selote","year":"2018","journal-title":"Plant Cell Environ."},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Rodr\u00edguez-Garc\u00eda, A., Morales, M.L., Garrido-Garc\u00eda, V., Garc\u00eda-Baquero, I., Leivas, A., Carre\u00f1o-Tarragona, G., S\u00e1nchez, R., Arenas, A., Cedena, T., and Ayala, R.M. (2019). Protein Carbonylation in Patients with Myelodysplastic Syndrome: An Opportunity for Deferasirox Therapy. Antioxidants, 8.","DOI":"10.3390\/antiox8110508"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"4295","DOI":"10.1093\/jxb\/erx194","article-title":"The role of Arabidopsis aldehyde dehydrogenase genes in response to high temperature and stress combinations","volume":"68","author":"Zhao","year":"2017","journal-title":"J. Exp. Bot."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"876","DOI":"10.1039\/C7MT00152E","article-title":"BRUTUS and its paralogs, BTS LIKE1 and BTS LIKE2, encode important negative regulators of the iron deficiency response in Arabidopsis thaliana","volume":"9","author":"Hindt","year":"2017","journal-title":"Metallomics"},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Li, Z.-G. (2019). Measurement of Signaling Molecules Calcium Ion, Reactive Sulfur Species, Reactive Carbonyl Species, Reactive Nitrogen Species, and Reactive Oxygen Species in Plants. Plant Signal. Mol. Role Regul. Under Stress. Environ., 83\u2013103.","DOI":"10.1016\/B978-0-12-816451-8.00005-8"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1016\/j.tplants.2014.11.004","article-title":"Molecular mechanisms governing Arabidopsis iron uptake","volume":"20","author":"Brumbarova","year":"2015","journal-title":"Trends Plant Sci."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"110604","DOI":"10.1016\/j.plantsci.2020.110604","article-title":"Jasmonic acid promotes leaf senescence through MYC2-mediated repression of CATALASE2 expression in Arabidopsis","volume":"299","author":"Zhang","year":"2020","journal-title":"Plant Sci."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"1869","DOI":"10.1111\/pce.13998","article-title":"Low nitrate alleviates iron deficiency by regulating iron homeostasis in apple","volume":"44","author":"Sun","year":"2021","journal-title":"Plant, Cell Environ."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.envexpbot.2013.03.006","article-title":"Iron deprivation-induced reactive oxygen species generation leads to non-autolytic PCD in Brassica napus leaves","volume":"91","author":"Tewari","year":"2013","journal-title":"Environ. Exp. Bot."},{"key":"ref_85","first-page":"e1108","article-title":"Histochemical Detection of Superoxide and H2O2 Accumulation in Brassica juncea Seedlings","volume":"8","author":"Kumar","year":"2014","journal-title":"Bio-Protocol"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/0003-9861(68)90654-1","article-title":"Photoperoxidation in isolated chloroplasts","volume":"125","author":"Heath","year":"1968","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/j.plaphy.2005.01.007","article-title":"Effects of temperature on oxidative stress defense systems, lipid peroxidation and lipoxygenase activity in Phalaenopsis","volume":"43","author":"Ali","year":"2005","journal-title":"Plant Physiol. Biochem."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"e1913","DOI":"10.21769\/BioProtoc.1913","article-title":"Measurements of Proline and Malondialdehyde Content and Antioxidant Enzyme Activities in Leaves of Drought Stressed Cotton","volume":"6","author":"Chen","year":"2016","journal-title":"Bio-Protocol"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"3778","DOI":"10.1016\/j.jprot.2012.04.046","article-title":"Analysis of oxidative stress-induced protein carbonylation using fluorescent hydrazides","volume":"75","author":"Tamarit","year":"2012","journal-title":"J. Proteom."},{"key":"ref_91","first-page":"4999","article-title":"Proteome-wide analysis of hydrogen peroxide-induced protein carbonylation in Arabidopsis thaliana","volume":"13","author":"Tola","year":"2022","journal-title":"Front. Plant Sci."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00425-023-04083-6","article-title":"Ammonium sulfate-based prefractionation improved proteome coverage and detection of carbonylated proteins in Arabidopsis thaliana leaf extract","volume":"257","author":"Tola","year":"2023","journal-title":"Planta"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/11\/9732\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:48:01Z","timestamp":1760125681000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/11\/9732"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,4]]},"references-count":92,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2023,6]]}},"alternative-id":["ijms24119732"],"URL":"https:\/\/doi.org\/10.3390\/ijms24119732","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,4]]}}}