{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T21:54:59Z","timestamp":1791928499363,"version":"4.3.4"},"reference-count":93,"publisher":"MDPI AG","issue":"18","license":[{"start":{"date-parts":[[2022,9,15]],"date-time":"2022-09-15T00:00:00Z","timestamp":1663200000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Scientific Cooperation between the Bulgarian Academy of Sciences and the Aristotle University of Thessaloniki","award":["2017\/01\/X\/ST4\/00373"],"award-info":[{"award-number":["2017\/01\/X\/ST4\/00373"]}]},{"name":"National Science Center in Poland","award":["2017\/01\/X\/ST4\/00373"],"award-info":[{"award-number":["2017\/01\/X\/ST4\/00373"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>Clary sage (Salvia sclarea L.) is a medicinal plant that has the potential to be used for phytoextraction of zinc (Zn) and cadmium (Cd) from contaminated soils by accumulating these metals in its tissues. Additionally, it has been found to be more tolerant to excess Zn than to Cd stress alone; however, the interactive effects of the combined treatment with Zn and Cd on this medicinal herb, and the protective strategies of Zn to alleviate Cd toxicity have not yet been established in detail. In this study, clary sage plants grown hydroponically were simultaneously exposed to Zn (900 \u00b5M) and Cd (100 \u03bcM) for 8 days to obtain more detailed information about the plant responses and the role of excess Zn in mitigating Cd toxicity symptoms. The leaf anatomy, photosynthetic pigments, total phenolic and anthocyanin contents, antioxidant capacity (by DPPH and FRAP analyses), and the uptake and distribution of essential elements were investigated. The results showed that co-exposure to Zn and Cd leads to an increased leaf content of Fe and Mg compared to the control, and to increased leaf Ca, Mn, and Cu contents compared to plants treated with Cd only. This is most likely involved in the defense mechanisms of excess Zn against Cd toxicity to protect the chlorophyll content and the functions of both photosystems and the oxygen-evolving complex. The data also revealed that the leaves of clary sage plants subjected to the combined treatment have an increased antioxidant capacity attributed to the higher content of polyphenolic compounds. Furthermore, light microscopy indicated more alterations in the leaf morphology after Cd-only treatment than after the combined treatment. The present study shows that excess Zn could mitigate Cd toxicity in clary sage plants.<\/jats:p>","DOI":"10.3390\/plants11182407","type":"journal-article","created":{"date-parts":[[2022,9,16]],"date-time":"2022-09-16T01:35:10Z","timestamp":1663292110000},"page":"2407","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":32,"title":["Combined Impact of Excess Zinc and Cadmium on Elemental Uptake, Leaf Anatomy and Pigments, Antioxidant Capacity, and Function of Photosynthetic Apparatus in Clary Sage (Salvia sclarea L.)"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7326-3771","authenticated-orcid":false,"given":"Anelia","family":"Dobrikova","sequence":"first","affiliation":[{"name":"Institute of Biophysics and Biomedical Engineering, Bulgarian Academy of Sciences, 1113 Sofia, Bulgaria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2081-4530","authenticated-orcid":false,"given":"Emilia","family":"Apostolova","sequence":"additional","affiliation":[{"name":"Institute of Biophysics and Biomedical Engineering, Bulgarian Academy of Sciences, 1113 Sofia, Bulgaria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9200-0862","authenticated-orcid":false,"given":"Ioannis-Dimosthenis S.","family":"Adamakis","sequence":"additional","affiliation":[{"name":"Section of Botany, Department of Biology, National and Kapodistrian University of Athens, 15784 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7524-2897","authenticated-orcid":false,"given":"Anetta","family":"Han\u0107","sequence":"additional","affiliation":[{"name":"Department of Trace Analysis, Faculty of Chemistry, Adam Mickiewicz University, 61-614 Poznan, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8755-0421","authenticated-orcid":false,"given":"Ilektra","family":"Sperdouli","sequence":"additional","affiliation":[{"name":"Institute of Plant Breeding and Genetic Resources, Hellenic Agricultural Organisation\u2013Demeter, Thermi, 57001 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0480-9387","authenticated-orcid":false,"given":"Michael","family":"Moustakas","sequence":"additional","affiliation":[{"name":"Department of Botany, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,9,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Alloway, B.J. (2013). Heavy Metals in Soils: Trace Metals and Metalloids in Soils and Their Bioavailability, Springer.","DOI":"10.1007\/978-94-007-4470-7"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Wu, F., Fan, J., Ye, X., Yang, L., Hu, R., Ma, J., Ma, S., Li, D., Zhou, J., and Nie, G. (2022). Unraveling cadmium toxicity in Trifolium repens L. seedling: Insight into regulatory mechanisms using comparative transcriptomics combined with physiological analyses. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23094612"},{"key":"ref_3","unstructured":"Hasanuzzaman, M., Prasad, M.N.V., and Fujita, M. (2019). Damage and protection of the photosynthetic apparatus under cadmium stress. Cadmium Toxicity and Tolerance in Plants: From Physiology to Remediation, Academic Press. [1st ed.]."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"773815","DOI":"10.3389\/fpls.2022.773815","article-title":"Cadmium Phytotoxicity, Tolerance, and Advanced Remediation Approaches in Agricultural Soils; A Comprehensive Review","volume":"13","author":"Zulfiqar","year":"2022","journal-title":"Front. Plant Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2115","DOI":"10.1093\/jexbot\/52.364.2115","article-title":"Cadmium-induced changes in the growth and oxidative metabolism of pea plants","volume":"52","author":"Sandalio","year":"2001","journal-title":"J. Exp. Bot."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.ecoenv.2016.04.001","article-title":"Cadmium minimization in wheat: A critical review","volume":"130","author":"Rizwan","year":"2016","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.plaphy.2017.02.015","article-title":"The wheat mutant DELLA-encoding gene (Rht-B1c) affects plant photosynthetic responses to cadmium stress","volume":"114","author":"Dobrikova","year":"2017","journal-title":"Plant Physiol. Biochem."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Adamakis, I.-D.S., Sperdouli, I., Hanc, A., Dobrikova, A., Apostolova, E., and Moustakas, M. (2021). Rapid hormetic responses of photosystem II photochemistry of clary sage to cadmium exposure. Int. J. Mol. Sci., 22.","DOI":"10.20944\/preprints202011.0283.v1"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1055\/s-2005-837696","article-title":"Ultrastructure and lipid alterations induced by cadmium in tomato (Lycopersicon esculentum) chloroplast membranes","volume":"7","author":"Djebali","year":"2005","journal-title":"Plant Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1631","DOI":"10.1556\/CRC.35.2007.4.10","article-title":"Cadmium-induced changes in the membrane lipid composition of maize plants","volume":"35","author":"Pal","year":"2007","journal-title":"Cereal Res. Commun."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1016\/j.ecoenv.2017.06.006","article-title":"Photosynthetic, antioxidative, molecular and ultrastructural responses of young cacao plants to Cd toxicity in the soil","volume":"144","author":"Mangabeira","year":"2017","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1122","DOI":"10.1111\/j.1365-3040.2004.01217.x","article-title":"Cd-induced subcellular accumulation of O2.\u2212 and H2O2 in pea leaves","volume":"27","author":"Corpas","year":"2004","journal-title":"Plant Cell Environ."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1080\/15226514.2013.828018","article-title":"Effective phytoextraction of cadmium (Cd) with increasing concentration of total phenolics and free proline in Cannabis sativa (L) plant under various treatments of fertilizers, plant growth regulators and sodium salt","volume":"17","author":"Ahmad","year":"2015","journal-title":"Int. J. Phytoremediat."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"652","DOI":"10.32615\/ps.2021.059","article-title":"Zinc and cadmium as modulating factors of the morphophysiological responses of Alternanthera tenella Colla (Amaranthaceae) under in vitro conditions","volume":"59","author":"Clairvil","year":"2021","journal-title":"Photosynthetica"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1007\/s12011-019-01974-2","article-title":"Heavy metal levels and mineral nutrient status in different parts of various medicinal plants collected from Eastern Mediterranean region of Turkey","volume":"197","author":"Karahan","year":"2020","journal-title":"Biol. Trace Elem. Res."},{"key":"ref_16","unstructured":"Marschner, H. (2012). Introduction, definition and classification of nutrients. Marschner\u2019s Mineral Nutrition of Higher Plants, Academic Press."},{"key":"ref_17","first-page":"322","article-title":"Zinc in plants\u2014An overview","volume":"24","author":"Tsonev","year":"2012","journal-title":"Emir. J. Food Agric."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1007\/s11627-015-9739-0","article-title":"In vitro plant regeneration of Ocimum basilicum L. is accelerated by zinc sulfate","volume":"52","author":"Verma","year":"2016","journal-title":"Vitr. Cell. Dev. Biol.-Plant"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.jhazmat.2018.01.040","article-title":"Zinc, zinc nanoparticles and plants","volume":"349","author":"Sturikova","year":"2018","journal-title":"J. Hazard. Mater."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2840","DOI":"10.1007\/s11356-016-8048-4","article-title":"Cadmium-zinc accumulation and photosystem II responses of Noccaea caerulescens to Cd and Zn exposure","volume":"24","author":"Moustaka","year":"2017","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3361","DOI":"10.1007\/s11356-014-3849-9","article-title":"Too much is bad\u2014An appraisal of phytotoxicity of elevated plant-beneficial heavy metal ions","volume":"22","author":"Anjum","year":"2015","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"748","DOI":"10.3389\/fpls.2019.00748","article-title":"Toxic Effects of Cd and Zn on the photosynthetic apparatus of the Arabidopsis halleri and Arabidopsis arenosa pseudo-metallophytes","volume":"10","author":"Sitko","year":"2019","journal-title":"Front. Plant Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"528","DOI":"10.1016\/j.ecoenv.2015.09.011","article-title":"Zinc-cadmium interactions: Impact on wheat physiology and mineral acquisition","volume":"122","author":"Sarwar","year":"2015","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1663","DOI":"10.1007\/s12665-013-2570-1","article-title":"Effectiveness of zinc application to minimize cadmium toxicity and accumulation in wheat (Triticum aestivum L.)","volume":"71","author":"Saifullah","year":"2014","journal-title":"Environ. Earth Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"862","DOI":"10.1071\/CP21598","article-title":"Growth, metal partitioning and antioxidant enzyme activities of mung beans as influenced by zinc oxide nanoparticles under cadmium stress","volume":"73","author":"Rashid","year":"2022","journal-title":"Crop Pasture Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"114979","DOI":"10.1016\/j.envpol.2020.114979","article-title":"Zinc alleviates cadmium toxicity by modulating photosynthesis, ROS homeostasis, and cation flux kinetics in rice","volume":"265","author":"Adil","year":"2020","journal-title":"Environm. Pollut."},{"key":"ref_27","first-page":"100405","article-title":"Evaluation of phytoremediation potential of aromatic plants: A systematic review","volume":"31","author":"Mishra","year":"2022","journal-title":"J. Appl. Res. Med. Aromat. Plants"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1016\/S1572-5995(02)80012-6","article-title":"Pharmacological activities and applications of Salvia sclarea and Salvia desoleana essential oils","volume":"26","author":"Peana","year":"2002","journal-title":"Stud. Nat. Prod. Chem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1438","DOI":"10.3390\/molecules14041438","article-title":"Chemical composition and biological activities of essential oil from Salvia sclarea plants regenerated in vitro","volume":"14","author":"Kalemba","year":"2009","journal-title":"Molecules"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1016\/j.lwt.2018.10.066","article-title":"Evaluation of some Turkish Salvia species by principal component analysis based on their vitamin B2, mineral composition, and antioxidant properties","volume":"100","author":"Gezek","year":"2019","journal-title":"LWT"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"111851","DOI":"10.1016\/j.ecoenv.2020.111851","article-title":"Cadmium toxicity in Salvia sclarea L.: An integrative response of element uptake, oxidative stress markers, leaf structure and photosynthesis","volume":"209","author":"Dobrikova","year":"2021","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"194","DOI":"10.3390\/plants10020194","article-title":"Tolerance mechanisms of the aromatic and medicinal plant Salvia sclarea L. to excess zinc","volume":"10","author":"Dobrikova","year":"2021","journal-title":"Plants"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Sperdouli, I., Adamakis, I.-D.S., Dobrikova, A., Apostolova, E., Han\u0107, A., and Moustakas, M. (2022). Excess zinc supply reduces cadmium uptake and mitigates cadmium toxicity effects on chloroplast structure, oxidative stress and photosystem II photochemical efficiency in Salvia sclarea plants. Toxics, 10.","DOI":"10.3390\/toxics10010036"},{"key":"ref_34","first-page":"780","article-title":"Potential of Salvia sclarea L. for phytoremediation of soils contaminated with heavy metals","volume":"10","author":"Angelova","year":"2016","journal-title":"Int. J. Agric. Biosyst. Eng."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1111\/plb.12665","article-title":"Leaf cell membrane stability-based mechanisms of zinc nutrient in mitigating salinity stress in rice","volume":"20","author":"Tufail","year":"2018","journal-title":"Plant Biol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1007\/s10646-013-1073-x","article-title":"Salicylic acid alleviates copper toxicity in rice (Oryza sativa L.) seedlings by up-regulating antioxidative and glyoxalase systems","volume":"22","author":"Mostofa","year":"2013","journal-title":"Ecotoxicology"},{"key":"ref_37","first-page":"1307","article-title":"Determination of the antioxidant capacity of Sideritis scardica specimens collected at different regions, C.R","volume":"69","author":"Shtereva","year":"2010","journal-title":"Acad. Bulg. Sci."},{"key":"ref_38","first-page":"618","article-title":"Determination of total phenolics and ascorbic acid related to an antioxidant activity and thermal stability of the Mao fruit juice","volume":"22","author":"Sripakdee","year":"2015","journal-title":"Int. Food Res. J."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.envexpbot.2018.01.006","article-title":"High anthocyanin accumulation in poinsettia leaves is accompanied by thylakoid membrane unstacking, acting as a photoprotective mechanism, to prevent ROS formation","volume":"154","author":"Moustaka","year":"2018","journal-title":"Environ. Exp. Bot."},{"key":"ref_40","first-page":"49","article-title":"Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis","volume":"Volume 100","author":"Schulze","year":"1994","journal-title":"Ecophysiology of Photosynthesis"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Moustakas, M., Bay\u00e7u, G., Sperdouli, I., Ero\u011flu, H., and Eleftheriou, E.P. (2020). Arbuscular mycorrhizal symbiosis enhances photosynthesis in the medicinal herb Salvia fruticosa by improving photosystem II photochemistry. Plants, 9.","DOI":"10.3390\/plants9080962"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Sperdouli, I., Andreadis, S., Moustaka, J., Panteris, E., Tsaballa, A., and Moustakas, M. (2021). Changes in light energy utilization in photosystem II and reactive oxygen species generation in potato leaves by the pinworm Tuta absoluta. Molecules, 26.","DOI":"10.3390\/molecules26102984"},{"key":"ref_43","first-page":"57","article-title":"An equipment for investigations of photosynthetic oxygen production reactions","volume":"28","author":"Zeinalov","year":"2002","journal-title":"Bulg. J. Plant Physiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1007\/s11120-019-00648-3","article-title":"Water oxidation in photosystem II","volume":"142","author":"Lubitz","year":"2019","journal-title":"Photosynth. Res."},{"key":"ref_45","unstructured":"Zeinalov, Y. (2010). Photosynthesis\u2014Behind the Fundamental Concepts, LAP Lambert Academic Publishing AG & Co. KG."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1007\/s40626-018-0102-9","article-title":"Improvement of the rice photosynthetic apparatus defence under cadmium stress modulated by salicylic acid supply to roots","volume":"30","author":"Yotsova","year":"2018","journal-title":"Theor. Exp. Plant Physiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.plaphy.2014.03.022","article-title":"Effects of exogenous 24-epibrassinolide on the photosynthetic membranes under non-stress conditions","volume":"80","author":"Dobrikova","year":"2014","journal-title":"Plant Physiol. Biochem."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.jplph.2015.06.008","article-title":"Damage and protection of the photosynthetic apparatus from UV-B radiation. II. Effect of quercetin at different pH","volume":"184","author":"Dobrikova","year":"2015","journal-title":"J. Plant Physiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/B978-0-12-385851-1.00001-9","article-title":"Heavy metal tolerance in Arabidopsis thaliana","volume":"60","author":"Chaffai","year":"2011","journal-title":"Adv. Bot. Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1093\/jxb\/erx465","article-title":"Trace metal metabolism in plants","volume":"69","author":"Andresen","year":"2018","journal-title":"J. Exp. Bot."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"710","DOI":"10.1016\/j.chemosphere.2016.12.116","article-title":"Phytoremediation strategies for soils contaminated with heavy metals: Modifications and future perspectives","volume":"171","author":"Sarwar","year":"2017","journal-title":"Chemosphere"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1483","DOI":"10.1007\/s11738-010-0687-3","article-title":"Growth and physiological responses of grape (Vitis vinifera \u201cCombier\u201d) to excess zinc","volume":"33","author":"Yang","year":"2011","journal-title":"Acta Physiol. Plant"},{"key":"ref_53","first-page":"23","article-title":"Effect of increasing zinc levels on Trigonella foenum-graecum growth and photosynthesis activity","volume":"95","author":"Melki","year":"2022","journal-title":"J. Appl. Bot. Food Qual."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"3115","DOI":"10.1093\/jxb\/erx063","article-title":"Impact of the ion transportome of chloroplasts on the optimization of photosynthesis","volume":"68","author":"Spetea","year":"2017","journal-title":"J. Exp. Bot."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"2013","DOI":"10.1093\/pcp\/pcq160","article-title":"Remodeling of the major light-harvesting antenna protein of PSII protects the young leaves of barley (Hordeum vulgare L.) from photoinhibition under prolonged iron deficiency","volume":"51","author":"Saito","year":"2010","journal-title":"Plant Cell Physiol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1519","DOI":"10.1007\/s00425-015-2276-6","article-title":"Iron- and manganese-assisted cadmium tolerance in Oryza sativa L.: Lowering of rhizotoxicity next to functional photosynthesis","volume":"241","author":"Sebastian","year":"2015","journal-title":"Planta"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1016\/j.bbabio.2015.02.010","article-title":"Calcium dependent regulation of photosynthesis","volume":"1847","author":"Hochmal","year":"2015","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Ahmad, P., Sarwat, M., Bhat, N.A., Wani, M.R., Kazi, A.G., and Tran, L.S.P. (2015). Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0114571"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1016\/S0981-9428(03)00035-4","article-title":"Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L.: A free floating freshwater macrophyte","volume":"41","author":"Aravind","year":"2003","journal-title":"Plant Physiol. Biochem."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"150992","DOI":"10.1016\/j.scitotenv.2021.150992","article-title":"Hormetic effects of zinc on growth and antioxidant defense system of wheat plants","volume":"807","author":"Wei","year":"2022","journal-title":"Sci. Total Environ."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1016\/j.indcrop.2012.08.029","article-title":"Evaluation of antioxidant activity, total phenols and phenolic compounds in thyme (Thymus vulgaris L.), sage (Salvia officinalis L.), and marjoram (Origanum majorana L.) extracts","volume":"43","author":"Roby","year":"2013","journal-title":"Ind. Crops Prod."},{"key":"ref_62","first-page":"223","article-title":"Phytochemical analysis and antioxidant evaluation of lemon grass (Cymbopogon citratus DC.) Stapf leaves","volume":"23","author":"Unuigbe","year":"2019","journal-title":"J. Appl. Sci. Environ. Manag."},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Francik, S., Francik, R., Sadowska, U., Bystrowska, B., Zawi\u015blak, A., Knapczyk, A., and Nzeyimana, A. (2020). Identification of phenolic compounds and determination of antioxidant activity in extracts and infusions of Salvia leaves. Materials, 13.","DOI":"10.3390\/ma13245811"},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Salinitro, M., Hoogerwerf, S., Casolari, S., Zappi, A., Melucci, D., and Tassoni, A. (2020). Production of antioxidant molecules in Polygonum aviculare (L.) and Senecio vulgaris (L.) under metal stress: A possible tool in the evaluation of plant metal tolerance. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21197317"},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Vidal, C., Ruiz, A., Ortiz, J., Larama, G., Perez, R., Santander, C., Ferreira, P., and Cornejo, P. (2020). Antioxidant responses of phenolic compounds and immobilization of copper in Imperata Cylindrica, a plant with potential use for bioremediation of Cu contaminated environments. Plants, 9.","DOI":"10.3390\/plants9101397"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1007\/s004250000400","article-title":"The involvement of polyphenols and peroxidase activities in heavy metal accumulation by epidermal glands of waterlily (Nympheaceae)","volume":"212","author":"Lavid","year":"2001","journal-title":"Planta"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/j.plaphy.2020.01.012","article-title":"Stress responses and nickel and zinc accumulation in different accessions of Stellaria media (L.) Vill. in response to solution pH variation in hydroponic culture","volume":"148","author":"Salinitro","year":"2020","journal-title":"Plant Physiol. Biochem."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1007\/s11738-012-1169-6","article-title":"Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants","volume":"35","author":"Sytar","year":"2013","journal-title":"Acta Physiol. Plant."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"104065","DOI":"10.1016\/j.envexpbot.2020.104065","article-title":"Anthocyanin accumulation in poinsettia leaves and its functional role in photo-oxidative stress","volume":"175","author":"Moustaka","year":"2020","journal-title":"Environ. Exp. Bot."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1016\/j.envexpbot.2015.05.012","article-title":"Multiple functional roles of anthocyanins in plant-environment interactions","volume":"119","author":"Landi","year":"2015","journal-title":"Env. Exp. Bot."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"109811","DOI":"10.1016\/j.ecoenv.2019.109811","article-title":"Modification of oxidative stress through changes in some indicators related to phenolic metabolism in Malva parviflora exposed to cadmium","volume":"187","author":"Zoufan","year":"2020","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/S0308-8146(01)00198-4","article-title":"Antioxidant activities of polyphenols from sage (Salvia officinalis)","volume":"75","author":"Lu","year":"2001","journal-title":"Food Chem."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1021\/jf025938l","article-title":"Quantitative kinetic analysis of hydrogen transfer reactions from dietary polyphenols to the DPPH radical","volume":"51","author":"Goupy","year":"2003","journal-title":"J. Agric. Food Chem."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1016\/j.foodchem.2004.08.020","article-title":"Antioxidant activity, total phenolic compounds of pistachio (Pistachia vera) hull extracts","volume":"92","author":"Goli","year":"2004","journal-title":"Food Chem."},{"key":"ref_75","first-page":"2585","article-title":"Antioxidant and antimicrobial activities of extract and essential oil of korarima Aframomum corrorima (Braun) P.C.M. Jansen)","volume":"7","author":"Eyob","year":"2008","journal-title":"Afr. J. Biotechnol."},{"key":"ref_76","first-page":"534","article-title":"Total phenolic content and antioxidant activity of kesum (Polygonum minus), ginger (Zingiber officinale) and turmeric (Curcuma longa) extract","volume":"18","author":"Maizura","year":"2001","journal-title":"Int. Food Res. J."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1016\/S0308-8146(03)00278-4","article-title":"4Free-radical scavenging capacity and antioxidant activity of selected plant species from the Canadian prairies","volume":"84","author":"Amarowicz","year":"2004","journal-title":"Food Chem."},{"key":"ref_78","first-page":"842","article-title":"Antioxidant properties of crude and fractionated extracts of Alpinia mutica rhizomes and their total phenolic content","volume":"5","author":"Phang","year":"2011","journal-title":"Afr. J. Pharm. Pharmacol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1134\/S1021443710060087","article-title":"Antioxidant capacity of sage grown on heavy metal-polluted soil","volume":"57","author":"Stancheva","year":"2010","journal-title":"Russ. J. Plant Physiol."},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Riyazuddin, R., Nisha, N., Ejaz, B., Khan, M.I.R., Kumar, M., Ramteke, P.W., and Gupta, R. (2021). A comprehensive review on the heavy metal toxicity and sequestration in plants. Biomolecules, 12.","DOI":"10.3390\/biom12010043"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.envexpbot.2005.06.012","article-title":"Localization and effects of cadmium in leaves of a cadmium-tolerant willow (Salix viminalis L.): Part II Microlocalization and cellular effects of cadmium","volume":"58","author":"Vollenweider","year":"2006","journal-title":"Environ. Exp. Bot."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1068","DOI":"10.1039\/b803602k","article-title":"Micro x-ray fluorescence imaging and micro x-ray absorption spectroscopy of cadmium hyper-accumulating plant, Arabidopsis halleri ssp. gemmifera, using high-energy synchrotron radiation","volume":"23","author":"Fukuda","year":"2008","journal-title":"J. Anal. Atom. Spectrom."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"712","DOI":"10.1111\/j.1469-8137.2008.02519.x","article-title":"Spatial distribution of cadmium in leaves of metal hyperaccumulating Thlaspi praecox using micro-PIXE","volume":"179","author":"Regvar","year":"2008","journal-title":"New Phytol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"1914","DOI":"10.1104\/pp.111.183947","article-title":"Cellular sequestration of cadmium in the hyperaccumulator plant species Sedum alfredii","volume":"157","author":"Tian","year":"2011","journal-title":"Plant Physiol."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Petrovic, D., and Krivokapic, S. (2020). The effect of Cu, Zn, Cd, and Pb accumulation on biochemical parameters (proline, chlorophyll) in the water caltrop (Trapa natans L.), Lake Skadar, Montenegro. Plants, 9.","DOI":"10.3390\/plants9101287"},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Yang, Y., Zhang, L., Huang, X., Zhou, Y., Quan, Q., Li, Y., and Zhu, X. (2020). Response of photosynthesis to different concentrations of heavy metals in Davidia involucrata. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0228563"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1007\/BF00402983","article-title":"Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins","volume":"170","author":"Demmig","year":"1987","journal-title":"Planta"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1007\/s11120-020-00726-x","article-title":"Effect of different light intensity on physiology, antioxidant capacity and photosynthetic characteristics on wheat seedlings under high CO2 concentration in a closed artificial ecosystem","volume":"144","author":"Yi","year":"2020","journal-title":"Photosynth. Res."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"3057","DOI":"10.1021\/bi015903z","article-title":"Reduction of the Mn cluster of the water-oxidizing enzyme by nitric oxide: Formation of an S-2 state","volume":"41","author":"Schansker","year":"2002","journal-title":"Biochemistry"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1007\/s00425-002-0808-3","article-title":"Electron flow to photosystem I from stromal reductants in vivo: The size of the pool of stromal reductants controls the rate of electron donation to both rapidly and slowly reducing photosystem I units","volume":"215","author":"Bukhov","year":"2002","journal-title":"Planta"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1007\/BF00020424","article-title":"The structure and function of the chloroplast photosynthetic membrane\u2014A model for the domain organization","volume":"46","author":"Albertsson","year":"1995","journal-title":"Photosynth. Res."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1198","DOI":"10.1016\/j.jplph.2005.08.020","article-title":"Changes in content and fatty acid profiles of total lipids of two halophytes: Sesuvium portulacastrum and Mesembryanthemum crystallinum under cadmium stress","volume":"163","author":"Nouairi","year":"2006","journal-title":"J. Plant Physiol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1007\/s12298-019-00734-9","article-title":"The cadmium-induced changes in the polar and neutral lipid compositions suggest the involvement of triacylglycerol in the defense response in maize","volume":"26","author":"Chaffai","year":"2020","journal-title":"Physiol. Mol. Biol. 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