{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T22:15:58Z","timestamp":1789683358715,"version":"4.0.1"},"reference-count":46,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2024,8,11]],"date-time":"2024-08-11T00:00:00Z","timestamp":1723334400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"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":["Plants"],"abstract":"<jats:p>We studied the recovery of the growth and physiological parameters of Scots pine seedlings after long-term zinc toxicity. The removal of excess zinc from the nutrient solution resulted in the rapid recovery of primary root growth but did not promote the initiation and growth of lateral roots. The recovery of root growth was accompanied by the rapid uptake of manganese, magnesium, and copper. Despite the maximum rate of manganese uptake by the roots, the manganese content in the needles of the recovering plants did not reach control values during the 28 days of the experiment, unlike magnesium, iron, and copper. In general, the recovery of ion homeostasis eliminated all of the negative effects on the photosynthetic pigment content in the needles. However, these changes, along with recovery of the water content in the needles, were not accompanied by an increase in the weight gain of the recovering seedlings compared with that of the Zn-stressed seedlings. The increased accumulation of phenolic compounds in the needles persisted for a long period after excess zinc was removed from the nutrient solution. The decreased lignin content in the roots and needles is a characteristic feature of Zn-stressed plants. Moreover, the removal of excess zinc from the nutrient solution did not lead to an increase in the lignin content in the organs.<\/jats:p>","DOI":"10.3390\/plants13162227","type":"journal-article","created":{"date-parts":[[2024,8,12]],"date-time":"2024-08-12T05:19:38Z","timestamp":1723439978000},"page":"2227","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Recovery of Scots Pine Seedlings from Long-Term Zinc Toxicity"],"prefix":"10.3390","volume":"13","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":"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":[[2024,8,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"113918","DOI":"10.1016\/j.envres.2022.113918","article-title":"Remediation Techniques for Elimination of Heavy Metal Pollutants from Soil: A Review","volume":"214","author":"Azhar","year":"2022","journal-title":"Environ. Res."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"131039","DOI":"10.1016\/j.jhazmat.2023.131039","article-title":"Comprehensive Mechanisms of Heavy Metal Toxicity in Plants, Detoxification, and Remediation","volume":"450","author":"Ghuge","year":"2023","journal-title":"J. Hazard. Mater."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"127970","DOI":"10.1016\/j.jhazmat.2021.127970","article-title":"Spatial Distribution of Toxic Metal (Loid) s at an Abandoned Zinc Smelting Site, Southern China","volume":"425","author":"Zeng","year":"2022","journal-title":"J. Hazard. Mater."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"8578","DOI":"10.1016\/j.biortech.2008.04.010","article-title":"Soil Contamination by Heavy Metals: Measurements from a Closed Unlined Landfill","volume":"99","author":"Kasassi","year":"2008","journal-title":"Bioresour. Technol."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Chmielowska-B\u0105k, J., and Deckert, J. (2021). Plant Recovery after Metal Stress\u2014A Review. Plants, 10.","DOI":"10.3390\/plants10030450"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Kosolapov, V.M., Cherniavskih, V.I., Dumacheva, E.V., Sajfutdinova, L.D., Zavalin, A.A., Glinushkin, A.P., Kosolapova, V.G., Kartabaeva, B.B., Zamulina, I.V., and Kalinitchenko, V.P. (2023). Scots Pine (Pinus sylvestris L.) Ecotypes Response to Accumulation of Heavy Metals during Reforestation on Chalk Outcrops. Forests, 14.","DOI":"10.3390\/f14071492"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Rahmonov, O., Sobala, M., \u015arodek, D., Karkosz, D., Pytel, S., and Rahmonov, M. (2024). The Spatial Distribution of Potentially Toxic Elements in the Mountain Forest Topsoils (the Silesian Beskids, Southern Poland). Sci. Rep., 14.","DOI":"10.1038\/s41598-023-50817-7"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1016\/j.jes.2022.06.015","article-title":"Spatial Heterogeneity and Source Apportionment of Soil Metal (Loid) s in an Abandoned Lead\/Zinc Smelter","volume":"127","author":"Zhang","year":"2023","journal-title":"J. Environ. Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1021\/es60042a001","article-title":"Contamination of Roadside Soil and Vegetation with Cadmium, Nickel, Lead, and Zinc","volume":"4","author":"Lagerwerff","year":"1970","journal-title":"Environ. Sci. Technol."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Yang, J., Zhao, Y., Ruan, X., and Zhang, G. (2023). Anthropogenic Contribution and Migration of Soil Heavy Metals in the Vicinity of Typical Highways. Agronomy, 13.","DOI":"10.3390\/agronomy13020303"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e8882","DOI":"10.1002\/ece3.8882","article-title":"Community Assembly during Vegetation Succession after Metal Mining Is Driven by Multiple Processes with Temporal Variation","volume":"12","author":"Li","year":"2022","journal-title":"Ecol. Evol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1007\/s11157-006-9117-9","article-title":"Industrial Barrens: Extreme Habitats Created by Non-Ferrous Metallurgy","volume":"6","author":"Kozlov","year":"2007","journal-title":"Rev. Environ. Sci. Biotechnol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"109751","DOI":"10.1016\/j.ecolind.2022.109751","article-title":"Bioactive Levels of Zn, Pb, Cu, Cd and Mg, Fe in Pollution Sensitive and Tolerant Scots Pines Needles\u2013Is Survival Mineral-Dependent?","volume":"146","author":"Diatta","year":"2023","journal-title":"Ecol. Indic."},{"key":"ref_14","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_15","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1007\/s10661-023-12134-4","article-title":"Adaptation of Betula Pendula Roth., Pinus sylvestris L., and Larix Decidua Mill. to Environmental Stress Caused by Tailings Waste Highly Contaminated by Trace Elements","volume":"196","author":"Kraj","year":"2024","journal-title":"Environ. Monit. Assess."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1007\/s10342-023-01637-x","article-title":"Which Trees Form the Best Soil? Reclaimed Mine Soil Properties under 22 Tree Species: 50 Years Later\u2014Assessment of Physical and Chemical Properties","volume":"143","author":"Vacek","year":"2024","journal-title":"Eur. J. For. Res."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Raklami, A., Meddich, A., Oufdou, K., and Baslam, M. (2022). Plants\u2014Microorganisms-Based Bioremediation for Heavy Metal Cleanup: Recent Developments, Phytoremediation Techniques, Regulation Mechanisms, and Molecular Responses. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23095031"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.1016\/j.envpol.2018.09.099","article-title":"Long-Term Impact of Cement Plant Emissions on the Elemental Composition of Both Soils and Pine Stands and on the Formation of Scots Pine Seeds","volume":"243","author":"Ivanov","year":"2018","journal-title":"Environ. Pollut."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1007\/BF00329030","article-title":"Maximum Rooting Depth of Vegetation Types at the Global Scale","volume":"108","author":"Canadell","year":"1996","journal-title":"Oecologia"},{"key":"ref_20","first-page":"845","article-title":"Pinus sylvestris in Europe: Distribution, Habitat, Usage and Threats","volume":"14","author":"Durrant","year":"2016","journal-title":"Eur. Atlas For. Tree Species"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1007\/s00468-006-0052-8","article-title":"Chemical Composition and Biochemical Changes in Needles of Scots Pine (Pinus sylvestris L.) Stands at Different Stages of Decline in Bulgaria","volume":"20","author":"Tzvetkova","year":"2006","journal-title":"Trees"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"970","DOI":"10.1007\/s10646-016-1654-6","article-title":"Accumulation of Heavy Metals and Antioxidant Responses in Pinus sylvestris L. Needles in Polluted and Non-Polluted Sites","volume":"25","author":"Barczyk","year":"2016","journal-title":"Ecotoxicology"},{"key":"ref_23","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_24","doi-asserted-by":"crossref","first-page":"14828","DOI":"10.1007\/s11356-020-11723-x","article-title":"Phytotoxicity of Short-Term Exposure to Excess Zinc or Copper in Scots Pine Seedlings in Relation to Growth, Water Status, Nutrient Balance, and Antioxidative Activity","volume":"28","author":"Ivanov","year":"2021","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1007\/s11738-016-2277-5","article-title":"Water Relations in Plants Subjected to Heavy Metal Stresses","volume":"38","year":"2016","journal-title":"Acta Physiol. Plant"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1093\/treephys\/17.1.39","article-title":"Responses of Picea, Pinus and Pseudotsuga Roots to Heterogeneous Nutrient Distribution in Soil","volume":"17","author":"George","year":"1997","journal-title":"Tree Physiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1111\/j.1365-3040.1991.tb00949.x","article-title":"Zinc-induced Vacuolation in Root Meristematic Cells of Festuca rubra L","volume":"14","author":"Davies","year":"1991","journal-title":"Plant Cell Environ."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1007\/s00425-021-03642-z","article-title":"Zinc Toxicity in Plants: A Review","volume":"253","author":"Kaur","year":"2021","journal-title":"Planta"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.chemosphere.2006.10.018","article-title":"Heavy Metal Toxicity to Lemna Minor: Studies on the Time Dependence of Growth Inhibition and the Recovery after Exposure","volume":"67","author":"Drost","year":"2007","journal-title":"Chemosphere"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1007\/s10535-011-0018-6","article-title":"Strategies of Cadmium and Zinc Resistance in Willow by Regulation of Net Accumulation","volume":"55","author":"Landberg","year":"2011","journal-title":"Biol. Plant."},{"key":"ref_31","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_32","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_33","first-page":"9","article-title":"Lignin Biosynthesis and Accumulation in Response to Abiotic Stresses in Woody Plants","volume":"2","author":"Han","year":"2022","journal-title":"For. Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"6652","DOI":"10.1007\/s00344-023-10926-z","article-title":"Lignin: The Building Block of Defense Responses to Stress in Plants","volume":"42","author":"Yadav","year":"2023","journal-title":"J. Plant Growth Regul."},{"key":"ref_35","first-page":"211","article-title":"Activation of Phenylpropanoid Pathway in Legume Plants Exposed to Heavy Metals. Part I. Effects of Cadmium and Lead on Phenylalanine Ammonia-Lyase Gene Expression, Enzyme Activity and Lignin Content","volume":"58","author":"Deckert","year":"2011","journal-title":"Acta Biochim. Pol."},{"key":"ref_36","first-page":"410","article-title":"Influence of Urban Environment Originated Heavy Metals Pollution on the Content of Extractives, Cellulose and Lignin in the Oak Wood","volume":"71","author":"Krutul","year":"2010","journal-title":"Ann. Wars. Univ. Life Sci. SGGW. For. Wood Technol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Lim-Hing, S., Gandhi, K.J., and Villari, C. (2024). The Role of Manganese in Tree Defenses against Pests and Pathogens. Plant Physiol. Biochem., 210.","DOI":"10.1016\/j.plaphy.2024.108641"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/j.envexpbot.2018.10.016","article-title":"Water Deficit-Dependent Changes in Non-Structural Carbohydrate Profiles, Growth and Mortality of Pine and Spruce Seedlings in Hydroculture","volume":"157","author":"Ivanov","year":"2019","journal-title":"Environ. Exp. Bot."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1134\/S1021443724605767","article-title":"Selection of Suitable Methods for Sample Preparation and Desorbing Agents for Determination of Nutrient Contents in Scots Pine Roots","volume":"71","author":"Ivanov","year":"2024","journal-title":"Russ. J. Plant Physiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1231","DOI":"10.1016\/S0891-5849(98)00315-3","article-title":"Antioxidant Activity Applying an Improved ABTS Radical Cation Decolorization Assay","volume":"26","author":"Re","year":"1999","journal-title":"Free Radic. Biol. Med."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"144","DOI":"10.5344\/ajev.1965.16.3.144","article-title":"Colorimetry of Total Phenolics with Phosphomolybdic-Phosphotungstic Acid Reagents","volume":"16","author":"Singleton","year":"1965","journal-title":"Am. J. Enol. Vitic."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"4267","DOI":"10.1021\/jf980366j","article-title":"Critical Factors of Vanillin Assay for Catechins and Proanthocyanidins","volume":"46","author":"Sun","year":"1998","journal-title":"J. Agric. Food Chem."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.plaphy.2016.03.014","article-title":"Phenolic Compounds as Indicators of Drought Resistance in Shrubs from Patagonian Shrublands (Argentina)","volume":"104","author":"Varela","year":"2016","journal-title":"Plant Physiol. Biochem."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1277","DOI":"10.1104\/pp.108.3.1277","article-title":"Elicitor-Induced Spruce Stress Lignin (Structural Similarity to Early Developmental Lignins)","volume":"108","author":"Lange","year":"1995","journal-title":"Plant Physiol."},{"key":"ref_45","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_46","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1016\/0076-6879(87)48036-1","article-title":"[34] Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembranes","volume":"148","author":"Lichtenthaler","year":"1987","journal-title":"Methods Enzymol."}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/13\/16\/2227\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:34:54Z","timestamp":1760110494000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/13\/16\/2227"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,8,11]]},"references-count":46,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2024,8]]}},"alternative-id":["plants13162227"],"URL":"https:\/\/doi.org\/10.3390\/plants13162227","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,8,11]]}}}