Cadmium (Cd) or nickel (Ni) were applied as a foliar spray (1 µM solution over one month) to mimic air pollution and to monitor metabolic responses and oxidative stress in the pteridophyte species. Exogenous metals did not affect the metal content of the soil and had relatively little effect on the essential elements in leaves or rhizomes. The amounts of Cd and Ni were similar in treated leaves (7.2 µg Cd or 5.3 µg Ni/g DW in mature leaves compared with 0.4 µg Cd or 1.2 µg Ni/g DW in the respective control leaves), but Ni was more abundant in rhizomes (56.6 µg Ni or 3.4 µg Cd/g DW), resulting in a higher Cd translocation and bioaccumulation factor. The theoretical calculation revealed that ca. 4% of Cd and 5.5% of Ni from the applied solution per plant/pot was absorbed. Excess Cd induced stronger ROS production followed by changes in SOD and CAT activities, whereas nitric oxide (NO) stimulation was less intense, as detected by confocal microscopy. The hadrocentric vascular bundles in the petioles also showed higher ROS and NO signals under metal excess. This may be a sign of increased ROS formation, and high correlations were observed. Proteins and amino acids were stimulated by Cd or Ni application in individual organs, whereas phenols and flavonols were almost unaffected. The data suggest that even low levels of exogenous metals induce an oxidative imbalance, although no visible damage is observed, and that the responses of ferns to metals are similar to those of seed plants or algae.

Department of Analytical Chemistry Faculty of Chemical Technology University of Pardubice Studentská 573 HB D 532 10 Pardubice Czech Republic

Department of Biology University of Trnava Priemyselná 4 918 43 Trnava Slovakia

Department of Chemistry and Environmental Sciences University of Ss Cyril and Methodius J Herdu 2 917 01 Trnava Slovakia

Department of Physiology Faculty of Medicine Masaryk University Kamenice 753 5 625 00 Brno Czech Republic

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Karmakar D., Padhy P.K. Metals uptake from particulate matter through foliar transfer and their impact on antioxidant enzymes activity of S. robusta in a tropical forest, West Bengal, India. Arch. Environ. Contam. Toxicol. 2019;76:605–616. doi: 10.1007/s00244-019-00599-9. PubMed DOI

Kováčik J., Klejdus B., Štork F., Hedbavny J. Physiological responses of Tillandsia albida (Bromeliaceae) to long-term foliar metal application. J. Hazard. Mater. 2012;239–240:175–182. doi: 10.1016/j.jhazmat.2012.08.062. PubMed DOI

Loya-González D., López-Serna D., Alfaro-Barbosa J.M., López-Reyes A., González-Rodríguez H., Cantú-Silva I. Chemical composition of bulk precipitation and its toxicity potential index in the metropolitan area of Monterrey, Northeastern Mexico. Environments. 2020;7:106. doi: 10.3390/environments7120106. DOI

Zha Y., Tang J., Pan Y. The effects of simulated acid rain and cadmium-containing atmospheric fine particulate matter on the pakchoi (Brassica campestris L.) seedlings growth and physiology. Soil Sci. Plant Nutr. 2022;68:317–328. doi: 10.1080/00380768.2021.2023826. DOI

Kováčik J., Babula P., Peterková V., Hedbavny J. Long-term impact of cadmium shows little damage in Scenedesmus acutiformis cultures. Algal Res. 2017;25:184–190. doi: 10.1016/j.algal.2017.04.029. DOI

Nabaei M., Amooaghaie R. Melatonin and nitric oxide enhance cadmium tolerance and phytoremediation efficiency in Catharanthus roseus (L.) G. Don. Environ. Sci. Pollut. Res. 2020;27:6981–6994. doi: 10.1007/s11356-019-07283-4. PubMed DOI

Balestri M., Bottega S., Spanò C. Response of Pteris vittata to different cadmium treatments. Acta Physiol. Plant. 2014;36:767–775. doi: 10.1007/s11738-013-1454-z. DOI

Kováčik J., Klejdus B., Babula P., Hedbavny J. Age affects not only metabolome but also metal toxicity in Scenedesmus quadricauda cultures. J. Hazard. Mater. 2016;306:58–66. doi: 10.1016/j.jhazmat.2015.11.056. PubMed DOI

Kováčik J., Štěrbová D., Babula P., Švec P., Hedbávný J. Toxicity of naturally contaminated manganese soil to selected crops. J. Agric. Food Chem. 2014;62:7287–7296. doi: 10.1021/jf5010176. PubMed DOI

Sobati-Nasab Z., Alirezalu A., Noruzi P. Effect of foliar application of nickel on physiological and phytochemical characteristics of pot marigold (Calendula officinalis) J. Agric. Food Res. 2021;3:100108. doi: 10.1016/j.jafr.2021.100108. DOI

Pavlova D., Karadjova I. Toxic element profiles in selected medicinal plants growing on serpentines in Bulgaria. Biol. Trace Elem. Res. 2013;156:288–297. doi: 10.1007/s12011-013-9848-8. PubMed DOI

Kubicka K., Samecka-Cymerman A., Kolon K., Kosiba P., Kempers A.J. Chromium and nickel in Pteridium aquilinum from environments with various levels of these metals. Environ. Sci. Pollut. Res. 2015;22:527–534. doi: 10.1007/s11356-014-3379-5. PubMed DOI PMC

Yu H., Li S., Wang A., Kuang Y., Wang F., Xing F. Accumulation of heavy metals and As in the fern Blechnum orientale L. from Guangdong Province, Southern China. Water Air Soil Pollut. 2020;231:342. doi: 10.1007/s11270-020-04645-4. DOI

Zhao L., Li T., Yu H., Chen G., Zhang X., Zheng Z., Li J. Changes in chemical forms, subcellular distribution, and thiol compounds involved in Pb accumulation and detoxification in Athyrium wardii (Hook.) Environ. Sci. Pollut. Res. 2015;22:12676–12688. doi: 10.1007/s11356-015-4464-0. PubMed DOI

Zemanová V., Pavlíková D., Hnilička F., Pavlík M. Toxicity-induced physiological and metabolic changes in the shoots of Pteris cretica and Spinacia oleracea. Plants. 2021;10:2009. doi: 10.3390/plants10102009. PubMed DOI PMC

Török A., Gulyás Z., Szalai G., Kocsy G., Majdik C. Phytoremediation capacity of aquatic plants is associated with the degree of phytochelatin polymerization. J. Hazard. Mater. 2015;299:371–378. doi: 10.1016/j.jhazmat.2015.06.042. PubMed DOI

Fismes J., Echevarria G., Leclerc-Cessac E., Morel J.L. Uptake and transport of radioactive nickel and cadmium in three vegetables after wet aerial contamination. J. Environ. Qual. 2005;34:1497–1507. doi: 10.2134/jeq2004.0274. PubMed DOI

Li L., Zhang Y., Ippolito J.A., Xing W., Qiu K., Wang Y. Cadmium foliar application affects wheat Cd, Cu, Pb and Zn accumulation. Environ. Pollut. 2020;262:114329. doi: 10.1016/j.envpol.2020.114329. PubMed DOI

Zhou Y.M., Long S.S., Li B.Y., Huang Y.Y., Li Y.J., Yu J.Y., Du H.H., Khan S., Lei M. Enrichment of cadmium in rice (Oryza sativa L.) grown under different exogenous pollution sources. Environ. Sci. Pollut. Res. 2020;27:44249–44256. doi: 10.1007/s11356-020-10282-5. PubMed DOI

Kováčik J., Babula P. Fluorescence microscopy as a tool for visualization of metal-induced oxidative stress in plants. Acta Physiol. Plant. 2017;39:157. doi: 10.1007/s11738-017-2455-0. DOI

Gong L., Liu X.D., Zeng Y.Y., Tian X.Q., Li Y.L., Turner N.C., Fang X.W. Stomatal morphology and physiology explain varied sensitivity to abscisic acid across vascular plant lineages. Plant Physiol. 2021;186:782–797. doi: 10.1093/plphys/kiab090. PubMed DOI PMC

Drăghiceanu O.A., Popescu M., Soare L.C. Stress response to nickel in Asplenium scolopendrium L. and Dryopteris filix-mas (L.) Schott. [(accessed on 14 March 2019)];Current Trends in Natural Sciences. 2016 5:151–156. Available online: https://www.upit.ro/_document/11964/paper_22.pdf.

Liu Y., Wang H.B., Wong M.H., Ye Z.H. The role of arsenate reductase and superoxide dismutase in As accumulation in four Pteris species. Environ. Int. 2009;35:491–495. doi: 10.1016/j.envint.2008.07.012. PubMed DOI

Kováčik J., Babula P., Hedbavny J. Comparison of vascular and non-vascular aquatic plant as indicators of cadmium toxicity. Chemosphere. 2017;180:86–92. doi: 10.1016/j.chemosphere.2017.04.002. PubMed DOI

Dvorakova M., Pumprova K., Antonínová Ž., Rezek J., Haisel D., Ekrt L., Vanek T., Langhansova L. Nutritional and antioxidant potential of fiddleheads from European ferns. Foods. 2021;10:460. doi: 10.3390/foods10020460. PubMed DOI PMC

Deng G., Li M., Li H., Yin L., Li W. Exposure to cadmium causes declines in growth and photosynthesis in the endangered aquatic fern (Ceratopteris pteridoides) Aquat. Bot. 2014;112:23–32. doi: 10.1016/j.aquabot.2013.07.003. DOI

Wang Y., Gao S., He X., Li Y., Zhang Y., Chen W. Response of total phenols, flavonoids, minerals, and amino acids of four edible fern species to four shading treatments. PeerJ. 2020;8:e8354. doi: 10.7717/peerj.8354. PubMed DOI PMC

Kováčik J., Husáková L., Graziani G., Patočka J., Vydra M., Rouphael Y. Nickel uptake in hydroponics and elemental profile in relation to cultivation reveal variability in three Hypericum species. Plant Physiol. Biochem. 2022;185:357–367. doi: 10.1016/j.plaphy.2022.06.009. PubMed DOI

Döring S., Korhammer S., Oetken M., Markert B. Analysis of phytochelatins in plant matrices by pre-column derivatization, high-performance liquid chromatography and fluorescence-detection. Fresenius J. Anal. Chem. 2000;366:316–318. doi: 10.1007/s002160050062. PubMed DOI