{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,9]],"date-time":"2026-09-09T22:22:00Z","timestamp":1788992520545,"version":"build-2803163510"},"reference-count":45,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2026,1,4]],"date-time":"2026-01-04T00:00:00Z","timestamp":1767484800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation","doi-asserted-by":"publisher","award":["25-14-00234"],"award-info":[{"award-number":["25-14-00234"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012190","name":"Ministry of Science and Higher Education of the Russian Federation","doi-asserted-by":"publisher","award":["122042700044-6"],"award-info":[{"award-number":["122042700044-6"]}],"id":[{"id":"10.13039\/501100012190","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>Manganese (Mn) is a crucial micronutrient for plants. The impaired function of the oxygen-evolving complex in Photosystem II (PSII) due to Mn deficiency is believed to result in the overproduction of reactive oxygen species and the induction of an enzymatic antioxidant system. In our study, we investigated the effects of progressive Mn deficiency (the difference in Mn content between the needles of control and Mn-deficient plants increased from 17-fold at the beginning of the experiment to 59-fold at the end) on the activities of superoxide dismutase (SOD), catalase, ascorbate peroxidase, and guaiacol peroxidase in the roots and needles of Scots pine seedlings. We found that the soluble protein content in plant organs under Mn deficiency was maintained at a level comparable to that of the control. Regardless of the severity of Mn deficiency, the needles of the Mn-deficient plants presented twofold lower SOD activity than the needles of the control plants. These differences were observed even when Mn deficiency did not negatively affect plant growth. Additionally, the total SOD activity in the needles of both plant groups was determined solely by the activity of the Cu\/Zn-containing SOD isozymes. Compared with the control plants, Mn deficiency did not result in an increase in any of the studied H2O2-degrading enzymes in the needles of the seedlings. In contrast, the needles of the Mn-deficient plants presented a lower level of guaiacol peroxidase activity. Despite the inhibition of root growth, Mn deficiency led to changes in the balance of the enzymatic antioxidant system in plant roots. The data obtained suggest that the lack of activation of SOD and other antioxidant enzymes in Scots pine seedlings against the background of progressive Mn deficiency is due to the reduced ability of PSII to generate ROS under these conditions.<\/jats:p>","DOI":"10.3390\/biology15010101","type":"journal-article","created":{"date-parts":[[2026,1,5]],"date-time":"2026-01-05T08:40:53Z","timestamp":1767602453000},"page":"101","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Enzymatic Antioxidant Defense System of Scots Pine Seedlings Under Conditions of Progressive Manganese Deficiency"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1465-1720","authenticated-orcid":false,"given":"Yury V.","family":"Ivanov","sequence":"first","affiliation":[{"name":"K.A. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, 127276 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexandra I.","family":"Ivanova","sequence":"additional","affiliation":[{"name":"K.A. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, 127276 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8556-8719","authenticated-orcid":false,"given":"Alexander V.","family":"Kartashov","sequence":"additional","affiliation":[{"name":"K.A. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, 127276 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Galina V.","family":"Glushko","sequence":"additional","affiliation":[{"name":"K.A. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, 127276 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Polina P.","family":"Loginova","sequence":"additional","affiliation":[{"name":"K.A. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, 127276 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vladimir V.","family":"Kuznetsov","sequence":"additional","affiliation":[{"name":"K.A. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, 127276 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,1,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Schmidt, S.B., and Husted, S. (2019). The Biochemical Properties of Manganese in Plants. Plants, 8.","DOI":"10.3390\/plants8100381"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Alejandro, S., H\u00f6ller, S., Meier, B., and Peiter, E. (2020). Manganese in Plants: From Acquisition to Subcellular Allocation. Front. Plant Sci., 11.","DOI":"10.3389\/fpls.2020.00300"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"e16","DOI":"10.1017\/qpb.2025.10012","article-title":"Manganese Handling in Plants: Advances in the Mechanistic and Functional Understanding of Transport Pathways","volume":"6","author":"Meier","year":"2025","journal-title":"Quant. Plant Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1016\/j.tplants.2016.03.001","article-title":"Manganese Deficiency in Plants: The Impact on Photosystem II","volume":"21","author":"Schmidt","year":"2016","journal-title":"Trends Plant Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1007\/s00299-024-03297-6","article-title":"Micronutrient Deficiency-Induced Oxidative Stress in Plants","volume":"43","author":"Gupta","year":"2024","journal-title":"Plant Cell Rep."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1146\/annurev.pp.43.060192.000503","article-title":"Superoxide Dismutase and Stress Tolerance","volume":"43","author":"Bowler","year":"1992","journal-title":"Annu. Rev. Plant Physiol. Plant Mol. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Hasanuzzaman, M., Fotopoulos, V., Nahar, K., and Fujita, M. (2019). Superoxide Dismutases (SODs) and Their Role in Regulating Abiotic Stress Induced Oxidative Stress in Plants. Reactive Oxygen, Nitrogen and Sulfur Species in Plants, Wiley.","DOI":"10.1002\/9781119468677"},{"key":"ref_8","unstructured":"Marschner, P. (2012). Chapter 7-Function of Nutrients: Micronutrients. Marschner\u2019s Mineral Nutrition of Higher Plants (Third Edition), Academic Press."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1427","DOI":"10.1080\/01904169809365493","article-title":"Micronutrient Deficiency Changes Activities of Superoxide Dismutase and Ascorbate Peroxidase in Tobacco Plants","volume":"21","author":"Yu","year":"1998","journal-title":"J. Plant Nutr."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1239","DOI":"10.1080\/01904168609363524","article-title":"Evaluation of Catalase and Peroxidase Activity as Indicators of Fe and Mn Nutrition for Soybean","volume":"9","author":"Leidi","year":"1986","journal-title":"J. Plant Nutr."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1078\/0176-1617-00931","article-title":"Manganese Nutrition Effects on Tomato Growth, Chlorophyll Concentration, and Superoxide Dismutase Activity","volume":"161","author":"Shenker","year":"2004","journal-title":"J. Plant Physiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1986","DOI":"10.1104\/pp.109.150946","article-title":"Export of Vacuolar Manganese by AtNRAMP3 and AtNRAMP4 Is Required for Optimal Photosynthesis and Growth under Manganese Deficiency","volume":"152","author":"Lanquar","year":"2010","journal-title":"Plant Physiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3345","DOI":"10.1007\/s11738-013-1367-x","article-title":"Oxidative Stress and Antioxidant Responses of Mulberry (Morus alba) Plants Subjected to Deficiency and Excess of Manganese","volume":"35","author":"Tewari","year":"2013","journal-title":"Acta Physiol. Plant."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1084","DOI":"10.1104\/pp.99.3.1084","article-title":"Antioxidants and Manganese Deficiency in Needles of Norway Spruce (Picea abies L.) Trees","volume":"99","author":"Polle","year":"1992","journal-title":"Plant Physiol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Ivanov, Y.V., Pashkovskiy, P.P., Ivanova, A.I., Kartashov, A.V., and Kuznetsov, V.V. (2022). Manganese Deficiency Suppresses Growth and Photosynthetic Processes but Causes an Increase in the Expression of Photosynthetic Genes in Scots Pine Seedlings. Cells, 11.","DOI":"10.3390\/cells11233814"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1104\/pp.95.1.21","article-title":"Isolation, Purification, and Subcellular Localization of Isozymes of Superoxide Dismutase from Scots Pine (Pinus sylvestris L.) Needles 1","volume":"95","author":"Wingsle","year":"1991","journal-title":"Plant Physiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.plaphy.2016.02.014","article-title":"Effects of Zinc on Scots Pine (Pinus sylvestris L.) Seedlings Grown in Hydroculture","volume":"102","author":"Ivanov","year":"2016","journal-title":"Plant Physiol. Biochem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1046\/j.1469-8137.1999.00427.x","article-title":"Specific Leaf Area and Leaf Dry Matter Content as Alternative Predictors of Plant Strategies","volume":"143","author":"Wilson","year":"1999","journal-title":"New Phytol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Ji, R., Min, J., Wang, Y., Kronzucker, H.J., and Shi, W. (2022). The Role of Plant Growth Regulators in Modulating Root Architecture and Tolerance to High-Nitrate Stress in Tomato. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.864285"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Pashkovskiy, P., Ivanov, Y., Ivanova, A., Kartashov, A., Zlobin, I., Lyubimov, V., Ashikhmin, A., Bolshakov, M., Kreslavski, V., and Kuznetsov, V. (2023). Effect of Light of Different Spectral Compositions on pro\/Antioxidant Status, Content of Some Pigments and Secondary Metabolites and Expression of Related Genes in Scots Pine. Plants, 12.","DOI":"10.3390\/plants12132552"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1016\/0003-2697(71)90370-8","article-title":"Superoxide Dismutase: Improved Assays and an Assay Applicable to Acrylamide Gels","volume":"44","author":"Beauchamp","year":"1971","journal-title":"Anal. Biochem."},{"key":"ref_22","first-page":"9780470110171","article-title":"Assay of Catalases and Peroxidases","volume":"10","author":"Chance","year":"1955","journal-title":"Methods Biochem. Anal."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1489","DOI":"10.1104\/pp.103.020396","article-title":"Properties of Guaiacol Peroxidase Activities Isolated from Corn Root Plasma Membranes","volume":"132","author":"Mika","year":"2003","journal-title":"Plant Physiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"867","DOI":"10.1093\/oxfordjournals.pcp.a076232","article-title":"Hydrogen Peroxide Is Scavenged by Ascorbate-Specific Peroxidase in Spinach Chloroplasts","volume":"22","author":"Nakano","year":"1981","journal-title":"Plant Cell Physiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1016\/0003-2697(78)90749-2","article-title":"A Simple Method for Quantitative, Semiquantitative, and Qualitative Assay of Protein","volume":"89","author":"Esen","year":"1978","journal-title":"Anal. Biochem."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Haider, S.R., Reid, H.J., and Sharp, B.L. (2012). Tricine-Sds-Page. Protein Electrophoresis: Methods and Protocols, Humana Press.","DOI":"10.1007\/978-1-61779-821-4_8"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1016\/0003-9861(78)90218-7","article-title":"Inhibition of Superoxide Dismutases by Azide","volume":"189","author":"Misra","year":"1978","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1007\/s00468-010-0496-8","article-title":"Ontogenetic Differentiation between Mediterranean and Eurasian Pines (Sect. Pinus) at the Seedling Stage","volume":"25","author":"Climent","year":"2011","journal-title":"Trees"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1201\/9780824746728.ch16","article-title":"Protein Synthesis by Plants under Stressful Conditions","volume":"2","author":"Dubey","year":"1999","journal-title":"Handb. Plant Crop Stress"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1134\/S1021443712010098","article-title":"Scots Pine as a Model Plant for Studying the Mechanisms of Conifers Adaptation to Heavy Metal Action: 2. Functioning of Antioxidant Enzymes in Pine Seedlings under Chronic Zinc Action","volume":"59","author":"Ivanov","year":"2012","journal-title":"Russ. J. Plant Physiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"17332","DOI":"10.1007\/s11356-016-6929-1","article-title":"Effects of Copper Deficiency and Copper Toxicity on Organogenesis and Some Physiological and Biochemical Responses of Scots Pine (Pinus sylvestris L.) Seedlings Grown in Hydroculture","volume":"23","author":"Ivanov","year":"2016","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1006\/anbo.1998.0811","article-title":"Micronutrient Deficiency Influences Plant Growth and Activities of Superoxide Dismutases in Narrow-Leafed Lupins","volume":"83","author":"Yu","year":"1999","journal-title":"Ann. Bot."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"742","DOI":"10.1104\/pp.90.2.742","article-title":"Assay and Electrophoresis of Superoxide Dismutase from Red Spruce (Picea rubens Sarg.), Loblolly Pine (Pinus taeda L.), and Scotch Pine (Pinus sylvestris L.) A Method for Biomonitoring","volume":"90","author":"Tandy","year":"1989","journal-title":"Plant Physiol."},{"key":"ref_34","first-page":"859","article-title":"Isolation and Purification of Mitochondrial Mn-Superoxide Dismutase from the Gymnosperm Pinus sylvestris L.","volume":"35","author":"Streller","year":"1994","journal-title":"Plant Cell Physiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1007\/BF01089035","article-title":"Pinus sylvestris L. Needles Contain Extracellular CuZn Superoxide Dismutase","volume":"192","author":"Streller","year":"1994","journal-title":"Planta"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1016\/0003-9861(77)90386-1","article-title":"Superoxide Dismutase and Peroxidase: A Positive Activity Stain Applicable to Polyacrylamide Gel Electropherograms","volume":"183","author":"Misra","year":"1977","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1007\/s12011-009-8549-9","article-title":"Effects of Manganese Deficiency on Spectral Characteristics and Oxygen Evolution in Maize Chloroplasts","volume":"136","author":"Gong","year":"2010","journal-title":"Biol. Trace Elem. Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"109042","DOI":"10.1016\/j.plaphy.2024.109042","article-title":"Manganese Deficiency Alters Photosynthetic Electron Transport in Marchantia Polymorpha","volume":"215","author":"Hani","year":"2024","journal-title":"Plant Physiol. Biochem."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"e70392","DOI":"10.1111\/ppl.70392","article-title":"PSII Photoinhibition as a Protective Strategy: Maintaining an Oxidative State of PSI by Suppressing PSII Activity Under Environmental Stress","volume":"177","author":"Takeuchi","year":"2025","journal-title":"Physiol. Plant."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1093\/jxb\/49.323.931","article-title":"Multiple Forms of Extracellular Superoxide Dismutase in Needles, Stem Tissues and Seedlings of Scots Pine","volume":"49","author":"Schinkel","year":"1998","journal-title":"J. Exp. Bot."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"863","DOI":"10.1016\/S0981-9428(03)00135-9","article-title":"The Antioxidant Systems Vis-\u00e0-Vis Reactive Oxygen Species during Plant\u2013Pathogen Interaction","volume":"41","author":"Tommasi","year":"2003","journal-title":"Plant Physiol. Biochem."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"153884","DOI":"10.1016\/j.jplph.2022.153884","article-title":"Phenolic Peroxidases: Dull Generalists or Purposeful Specialists in Stress Responses?","volume":"280","year":"2023","journal-title":"J. Plant Physiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1191","DOI":"10.1093\/treephys\/14.10.1191","article-title":"Effects of Manganese Deficiency on Soluble Apoplastic Peroxidase Activities and Lignin Content in Needles of Norway Spruce (Picea abies)","volume":"14","author":"Polle","year":"1994","journal-title":"Tree Physiol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Skwarek, M., Patykowski, J., and Witczak, A. (2017). Changes in Antioxidant Enzyme Activities in Pinus sylvestris and Larix decidua Seedlings After Melolontha melolontha Attack, Forest Research Institute.","DOI":"10.1515\/frp-2017-0017"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2700","DOI":"10.1093\/jxb\/erae061","article-title":"Physiological Function and Regulation of Ascorbate Peroxidase Isoforms","volume":"75","author":"Yoshimura","year":"2024","journal-title":"J. Exp. Bot."}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/1\/101\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,1,5]],"date-time":"2026-01-05T08:57:22Z","timestamp":1767603442000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/1\/101"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,1,4]]},"references-count":45,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2026,1]]}},"alternative-id":["biology15010101"],"URL":"https:\/\/doi.org\/10.3390\/biology15010101","relation":{},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,1,4]]}}}