A pot experiment was undertaken to investigate the effect of Cd, Pb and Zn multi-contamination on the physiological and metabolic response of carrot (Daucus carota L.) after 98 days of growth under greenhouse conditions. Multi-contamination had a higher negative influence on leaves (the highest Cd and Zn accumulation) compared to the roots, which showed no visible change in terms of anatomy and morphology. The results showed the following: (i) significantly higher accumulation of Cd, Zn, and Pb in the multi-contaminated variant (Multi) compared to the control; (ii) significant metabolic responses-an increase in the malondialdehyde content of the Multi variant compared to the control in the roots (by 20%), as well as in the leaves (by 53%); carotenoid content in roots decreased by 31% in the Multi variant compared with the control; and changes in free amino acids, especially those related to plant stress responses. The determination of hydroxyproline and sarcosine may reflect the higher sensitivity of carrot leaves to multi-contamination in comparison to roots. A similar trend was observed for the content of free methionine (significant increase of 31% only in leaves); (iii) physiological responses (significant decreases in biomass, changes in gas-exchange parameters and chlorophyll a); and (iv) significant changes in enzymatic activities (chitinase, alanine aminopeptidase, acid phosphatase) in the root zone.

Department of Agroenvironmental Chemistry and Plant Nutrition Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamýcká 129 16500 Prague Czech Republic

Department of Botany and Plant Physiology Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamýcká 129 16500 Prague Czech Republic

Department of Soil Science and Soil Protection Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamýcká 129 16500 Prague Czech Republic

Zobrazit více v PubMed

Özcan M.M., Yılmaz F.G., Kulluk D.A. The accumulation of element and heavy metal concentrations in different parts of some carrot and radish types. Environ. Monit. Assess. 2023;195:754. doi: 10.1007/s10661-023-11364-w. PubMed DOI

Ahmad I., Ansari T.M. An assessment of toxic heavy metals in soil and plants (Allium cepa and Daucus carota) by GFAAS. Int. J. Environ. Anal. Chem. 2022;102:1029–1048. doi: 10.1080/03067319.2020.1730341. DOI

Hou S., Zheng N., Tang L., Ji X. Effects of cadmium and copper mixtures to carrot and pakchoi under greenhouse cultivation condition. Ecotoxicol. Environ. Saf. 2018;159:172–181. doi: 10.1016/j.ecoenv.2018.04.060. PubMed DOI

Pietrelli L., Menegoni P., Papetti P. Bioaccumulation of heavy metals by herbaceous species grown in urban and rural sites. Ecotoxicol. Environ. Saf. 2022;233:141. doi: 10.1007/s11270-022-05577-x. DOI

Kebonye N.M., Eze P.N., John K., Agyeman P.C., Němeček K., Borůvka L. An in-depth human health risk assessment of potentially toxic elements in highly polluted riverine soils, Příbram (Czech Republic) Environ. Geochem. Health. 2021;44:369–385. doi: 10.1007/s10653-021-00877-3. PubMed DOI

Gooday G.W. Physiology and microbial degradation of chitin and chitosan. In: Ratledge C., editor. Biochemstry of Microbial Degradation. Kluwer Academic Publishers; Dordrecht, The Netherlands: 1994. pp. 279–312.

Gao L., Smith A.R., Jones D.L., Guo Y., Liu B., Guo Z., Fan C.H., Zheng J., Cui X., Hill P.W. How do tree species with different successional stages affect soil organic nitrogen transformations? Geoderma. 2023;430:116319. doi: 10.1016/j.geoderma.2022.116319. DOI

Chowdhury N., Rasid M.M. Heavy metal concentrations and its impact on soil microbial and enzyme activities in agricultural lands around ship yards in Chattogram, Bangladesh. Soil Sci. Annu. 2021;72:135994. doi: 10.37501/soilsa/135994. DOI

Cui Y., Wang X., Wang X., Zhang X., Fang L. Evaluation methods of heavy metal pollution in soils based on enzyme activities: A review. Soil Ecol. Lett. 2021;3:169–177. doi: 10.1007/s42832-021-0096-0. DOI

Adetunji A.T., Lewu F.B., Mulidzi R., Ncube B. The biological activities of β-glucosidase, phosphatase and urease as soil quality indicators: A review. J. Soil Sci. Plant Nutr. 2017;17:794–807. doi: 10.4067/S0718-95162017000300018. DOI

Gupta N., Yadav K.K., Kumar V., Kumar S., Chadd R.P., Kumar A. Trace elements in soil-vegetables interface: Translocation, bioaccumulation, toxicity and amelioration—A review. Sci. Total Environ. 2019;651:2927–2942. doi: 10.1016/j.scitotenv.2018.10.047. PubMed DOI

Caracciolo B.A., Terenzi V. Rhizosphere microbial communities and heavy metals. Microorganisms. 2021;9:1462. doi: 10.3390/microorganisms9071462. PubMed DOI PMC

Seshadri B., Bolan N.S., Naidu R. Rhizosphere-induced heavy metal(loid) transformation in relation to bioavailability and remediation. J. Soil Sci. Plant Nutr. 2015;15:524–548. doi: 10.4067/S0718-95162015005000043. DOI

Bidar G., Pelfrêne A., Schwartz C.H., Waterlot C.H., Sahmer K., Marot F., Douay F. Urban kitchen gardens: Effect of the soil contamination and parameters on the trace element accumulation in vegetables—A review. Sci. Total Environ. 2020;738:139569. doi: 10.1016/j.scitotenv.2020.139569. PubMed DOI

Liu X., Ju Y., Mandzhieva S., Pinskii D., Minkina T., Rajput V.D., Roane T., Huang S., Li Y., Ma L.Q., et al. Sporadic Pb accumulation by plants: Influence of soil biogeochemistry, microbial community and physiological mechanisms. J. Hazard. Mater. 2023;444:130391. doi: 10.1016/j.jhazmat.2022.130391. PubMed DOI

Clemens S., Ma J.F. Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu. Rev. Plant Biol. 2016;67:489–512. doi: 10.1146/annurev-arplant-043015-112301. PubMed DOI

Asati A., Pichhode M., Nikhil K. Effect of heavy metals on plants: An overview. Int. J. Appl. Innov. Eng. Manag. 2016;5:56–66.

Viehweger K. How plants cope with heavy metals. Bot. Stud. 2014;55:35. doi: 10.1186/1999-3110-55-35. PubMed DOI PMC

Pavlíková D., Zemanová V., Procházková D., Pavlík M., Száková J., Wilhelmová N. The long-term effect of zinc soil contamination on selected free amino acids playing an important role in plant adaptation to stress and senescence. Ecotoxicol. Environ. Saf. 2014;100:166–170. doi: 10.1016/j.ecoenv.2013.10.028. PubMed DOI

Thakur S., Singh L., Wahid Z.A., Siddiqui M.F., Atnaw S.M., Din M.F.M. Plant-driven removal of heavy metals from soil: Uptake, translocation, tolerance mechanism, challenges, and future perspectives. Environ. Monit. Assess. 2016;188:206. doi: 10.1007/s10661-016-5211-9. PubMed DOI

Ovečka M., Takáč T. Managing heavy metal toxicity stress in plants: Biological and biotechnological tools. Biotechnol. Adv. 2014;32:73–86. doi: 10.1016/j.biotechadv.2013.11.011. PubMed DOI

Gao Y., Li H., Song Y., Zhang F., Yang Z., Yang Y., Grohmann T. Response of glutathione pools to cadmium stress and the strategy to translocate cadmium from roots to leaves (Daucus carota L.) Sci. Total Environ. 2022;823:153575. doi: 10.1016/j.scitotenv.2022.153575. PubMed DOI

Shahid M., Khalid S., Abbas G., Shahid N., Nadeem M., Sabir M., Aslam M., Dumat C. Heavy metal stress and crop productivity. In: Hakeem K.R., editor. Crop Production and Global Environmental Issues. Springer; Cham, Switzerland: 2015. pp. 1–25. DOI

Ghori N.-H., Ghori T., Hayat M.Q., Imadi S.R., Gul A., Altay V., Ozturk M. Heavy metal stress and responses in plants. Int. J. Environ. Sci. Technol. 2019;16:1807–1828. doi: 10.1007/s13762-019-02215-8. DOI

Gill M. Heavy metal stress in plants: A review. Int. J. Adv. Res. 2014;2:1043–1055.

Huang X., Duan S., Wu Q., Yu M., Shabala S. Reducing Cadmium accumulation in plants: Structure–function relations and tissue-specific operation of transporters in the spotlight. Plants. 2020;9:223. doi: 10.3390/plants9020223. PubMed DOI PMC

Yang Y., Chen W., Wang M., Li Y., Peng C. Evaluating the potential health risk of toxic trace elements in vegetables: Accounting for variations in soil factors. Sci. Total Environ. 2017;584:942–949. doi: 10.1016/j.scitotenv.2017.01.143. PubMed DOI

Zulfiqar U., Jiang W., Xiukang W., Hussain S., Ahmad M., Maqsood M.F., Ali N., Ishfaq M., Kaleem M., Haider F.U., et al. Cadmium phytotoxicity, tolerance, and advanced remediation approaches in agricultural soils; A comprehensive review. Front. Plant Sci. 2022;13:773815. doi: 10.3389/fpls.2022.773815. PubMed DOI PMC

Baruah N., Gogoi N., Roy S., Bora P., Chetia J., Zahra N., Ali N., Gogoi P., Farooq M. Phytotoxic responses and plant tolerance mechanisms to cadmium toxicity. J. Soil Sci. Plant Nutr. 2023:1–22. doi: 10.1007/s42729-023-01525-8. DOI

Hamzah Saleem M., Usman K., Rizwan M., Al Jabri H., Alsafran M. Functions and strategies for enhancing zinc availability in plants for sustainable agriculture. Front. Plant Sci. 2022;13:1033092. doi: 10.3389/fpls.2022.1033092. PubMed DOI PMC

Kaur H., Garg N. Zinc toxicity in plants: A review. Planta. 2021;253:129. doi: 10.1007/s00425-021-03642-z. PubMed DOI

Natasha N., Shahid M., Bibi I., Iqbal J., Khalid S., Murtaza B., Bakhat H.F., Farooq A.B.U., Amjad M., Hammad H.M., et al. Zinc in soil-plant-human system: A data-analysis review. Sci. Total Environ. 2022;808:152024. doi: 10.1016/j.scitotenv.2021.152024. PubMed DOI

Goodarzi A., Namdjoyan S., Soorki A.A. Effects of exogenous melatonin and glutathione on zinc toxicity in safflower (Carthamus tinctorius L.) seedlings. Ecotoxicol. Environ. Saf. 2020;201:110853. doi: 10.1016/j.ecoenv.2020.110853. PubMed DOI

Fahr M., Laplaze L., Bendaou N., Hocher V., El Mzibri M., Bogusz D., Smouni A. Effect of lead on root growth. Front. Plant Sci. 2013;4:175. doi: 10.3389/fpls.2013.00175. PubMed DOI PMC

Ghani M.A., Abbas M.M., Ali B., Aziz R., Qadri R.W.K., Noor A., Azam M., Bahzad S., Saleem M.H., Abualreesh M.H., et al. Alleviating role of gibberellic acid in enhancing plant growth and stimulating phenolic compounds in carrot (Daucus carota L.) under lead stress. Sustainability. 2021;13:12329. doi: 10.3390/su132112329. DOI

Collin S., Baskar A., Geevarghese D.M., Ali M.N.V.S., Bahubali P., Choudhary R., Lvov V., Tovar G.I., Senatov F., Koppala S., et al. Bioaccumulation of lead (Pb) and its effects in plants: A review. J. Hazard. Mater. 2022;3:100064. doi: 10.1016/j.hazl.2022.100064. DOI

Dogan M., Karatas M., Aasim M. Cadmium and lead bioaccumulation potentials of an aquatic macrophyte Ceratophyllum demersum L.: A laboratory study. Ecotoxicol. Environ. Saf. 2018;148:431–440. doi: 10.1016/j.ecoenv.2017.10.058. PubMed DOI

Khan A., Khan S., Khan M.A., Qamar Z., Waqas M. The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: A review. Environ. Sci. Pollut. Res. 2015;22:13772–13799. doi: 10.1007/s11356-015-4881-0. PubMed DOI

Guo Z., Gao Y., Yuan X., Yuan M., Huang L., Wang S., Liu C., Duan C. Effects of heavy metals on stomata in plants: A review. Int. J. Mol. Sci. 2023;24:9302. doi: 10.3390/ijms24119302. PubMed DOI PMC

Que F., Hou X.-L., Wang G.-L., Xu Z.-S., Tan G.-F., Li T., Wang Y.-H., Khadr A., Xiong A.-S. Advances in research on the carrot, an important root vegetable in the Apiaceae family. Hortic. Res. 2019;6:69. doi: 10.1038/s41438-019-0150-6. PubMed DOI PMC

Knez E., Kadac-Czapska K., Dmochowska-Ślęzak K., Grembecka M. Root vegetables—Composition, health effects, and contaminants. Int. J. Environ. Res. Public Health. 2022;19:15531. doi: 10.3390/ijerph192315531. PubMed DOI PMC

do Sousa Lima F., do Nascimento C.W.A., da Silva Sousa C. Lead and nutrient allocation in vegetables grown in soil from a battery site. Semin. Cienc. Agrar. 2015;36:2483–2491. doi: 10.5433/1679-0359.2015v36n4p2483. DOI

Roy M., McDonald L.M. Metal uptake in plants and health risk assessments in metal-contaminated smelter soils. Land Degrad. Dev. 2015;26:785–792. doi: 10.1002/ldr.2237. DOI

Stančić Z., Vujević D., Gomaz A., Bogdan S., Vincek D. Detection of heavy metals in common vegetables at Varaždin city market, Croatia. Arch. Ind. Hyg. Toxicol. 2016;67:340–350. doi: 10.1515/aiht-2016-67-2823. PubMed DOI

Andrejić G., Gajić G., Prica M., Dželetović Ž., Rakić T. Zinc accumulation, photosynthetic gas exchange, and chlorophyll a fluorescence in Zn-stressed Miscanthus × giganteus plants. Photosynthetica. 2018;56:1249–1258. doi: 10.1007/s11099-018-0827-3. DOI

Nedelescu M., Baconi D., Neagoe A., Iordache V., Stan M., Constantinescu P., Ciobanu A.M., Vardavas A.I., Vinceti M., Tsatsakis A.M. Environmental metal contamination and health impact assessment in two industrial regions of Romania. Sci. Total Environ. 2017;580:984–995. doi: 10.1016/j.scitotenv.2016.12.053. PubMed DOI

Bakhshayesh B.E., Delkash M., Scholz M. Response of vegetables to cadmium-enriched soil. Water. 2014;6:1246–1256. doi: 10.3390/w6051246. DOI

Yang D., Guo Z., Green I.D., Xie D. Effect of cadmium accumulation on mineral nutrient levels in vegetable crops: Potential implications for human health. Environ. Sci. Pollut. Res. 2016;23:19744–19753. doi: 10.1007/s11356-016-7186-z. PubMed DOI

Basu A., Mazumdar I., Goswami K. Concentrations of lead in selected vegetables grown & marketed along major highway in Kolkata (India) IIOAB J. 2013;4:32.

Lizarazo M.F., Herrera C.D., Celis C.A., Pombo L.M., Teherán A.A., Piñeros L.G., Rodríguez O.E. Contamination of staple crops by heavy metals in Sibaté, Colombia. Heliyon. 2020;6:e04212. doi: 10.1016/j.heliyon.2020.e04212. PubMed DOI PMC

O’Lexy R., Kasai K., Clark N., Fujiwara T., Sozzani R., Gallagher K.L. Exposure to heavy metal stress triggers changes in plasmodesmatal permeability via deposition and breakdown of callose. J. Exp. Bot. 2018;69:3715–3728. doi: 10.1093/jxb/ery171. PubMed DOI PMC

Massaccesi L., Meneghini C., Comaschi T., D’Amato R., Onofri A., Businelli D. Ligands involved in Pb immobilization and transport in lettuce, radish, tomato and Italian ryegrass. J. Plant Nutr. Soil Sci. 2014;177:766–774. doi: 10.1002/jpln.201200581. DOI

Orroño D.I., Schindler V., Lavado R.S. Heavy metal availability in Pelargonium hortorum rhizosphere: Interactions, uptake and plant accumulation. J. Plant Nutr. 2012;35:1374–1386. doi: 10.1080/01904167.2012.684129. DOI

Tran L.T.T., Luan L.V., Hieu T.Q., Van Tan L. Study on the effect of Cu (II) and Zn (II) on the accumulation of Pb (II) from soil to the biomass of vegetable. Int. J. Agron. 2021;2021:6687566. doi: 10.1155/2021/6687566. DOI

Woźniak A., Bednarski W., Dancewicz K., Gabryś B., Borowiak-Sobkowiak B., Bocianowski J., Samardakiewicz S., Rucińska-Sobkowiak R., Morkunas I. Oxidative stress links response to lead and Acyrthosiphon pisum in Pisum sativum L. J. Plant Physiol. 2019;240:152996. doi: 10.1016/j.jplph.2019.152996. PubMed DOI

Tirani M.M., Haghjou M.M. Reactive oxygen species (ROS), total antioxidant capacity (AOC) and malondialdehyde (MDA) make a triangle in evaluation of zinc stress extension. J. Anim. Plant Sci. 2019;29:1100–1111.

Hafizi Z., Nasr N. The effect of zinc oxide nanoparticles on safflower plant growth and physiology. Eng. Technol. Appl. Sci. Res. 2018;8:2508–2513. doi: 10.48084/etasr.1571. DOI

Zacchini M., Rea M., Tullio M., de Agazio M. Increased antioxidative capacity in maize calli during and after oxidative stress induced by a long lead treatment. Plant Physiol. Biochem. 2003;41:49–54. doi: 10.1016/S0981-9428(02)00008-6. DOI

Reddy A.M., Kumar S.G., Jyothsnakumari G., Thimmanaik S., Sudhakar C. Lead induced changes in antioxidant metabolism of horsegram (Macrotyloma uniflorum (Lam.) Verdc.) and bengalgram (Cicer arietinum L.) Chemosphere. 2005;60:97–104. doi: 10.1016/j.chemosphere.2004.11.092. PubMed DOI

Bharwana S.A., Ali S., Farooq M.A., Iqbal N., Abbas F., Ahmad M.S.A. Alleviation of lead toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes suppressed lead uptake and oxidative stress in cotton. J. Bioremediation Biodegrad. 2013;4:187. doi: 10.4172/2155-6199.1000187. PubMed DOI

An Q., He X., Zheng N., Hou S., Sun S., Wang S., Penyang L., Xiaoqian L., Song X. Physiological and genetic effects of cadmium and copper mixtures on carrot under greenhouse cultivation. Ecotoxicol. Environ. Saf. 2020;206:111363. doi: 10.1016/j.ecoenv.2020.111363. PubMed DOI

Lanier C., Bernard F., Dumez S., Leclercq-Dransart J., Lemiere S., Vandenbulcke F., Nesslany F., Platel A., Devred I., Hayet A., et al. Combined toxic effects and DNA damage to two plant species exposed to binary metal mixtures (Cd/Pb) Ecotoxicol. Environ. Saf. 2019;167:278–287. doi: 10.1016/j.ecoenv.2018.10.010. PubMed DOI

Rizvi A., Khan M.S. Heavy metal-induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and stress mitigation by metal tolerant nitrogen-fixing Azotobacter chroococcum. Ecotoxicol. Environ. Saf. 2018;157:9–20. doi: 10.1016/j.ecoenv.2018.03.063. PubMed DOI

Rosas-Saavedra C., Quiroz L.F., Parra S., Gonzalez-Calquin C., Arias D., Ocarez N., Lopez F., Stange C. Putative Daucus carota capsanthin-capsorubin synthase (DcCCS) possesses lycopene β-cyclase activity, boosts carotenoid levels, and increases salt tolerance in heterologous plants. Plants. 2023;12:2788. doi: 10.3390/plants12152788. PubMed DOI PMC

Faiz S., Yasin N.A., Khan W.U., Shah A.A., Akram W., Ahmad A., Ali A., Naveed N.H., Riaz L. Role of magnesium oxide nanoparticles in the mitigation of lead-induced stress in Daucus carota: Modulation in polyamines and antioxidant enzymes. Int. J. Phytoremediation. 2021;24:364–372. doi: 10.1080/15226514.2021.1949263. PubMed DOI

Sharma R.K., Agrawal M., Agrawal S.B. Physiological and biochemical responses resulting from cadmium and zinc accumulation in carrot plants. J. Plant Nutr. 2010;33:1066–1079. doi: 10.1080/01904161003729774. DOI

Majeed A., Muhammad Z., Siyar S. Assessment of heavy metal induced stress responses in pea (Pisum sativum L.) Acta Ecol. Sin. 2019;39:284–288. doi: 10.1016/j.chnaes.2018.12.002. DOI

Emamverdian A., Ding Y., Mokhberdoran F., Xie Y. Heavy metal stress and some mechanisms of plant defense response. Sci. World J. 2015;2015:756120. doi: 10.1155/2015/756120. PubMed DOI PMC

Faseela P., Sinisha A.K., Brestic M., Puthur J.T. Chlorophyll a fluorescence parameters as indicators of a particular abiotic stress in rice. Photosynthetica. 2020;58:293–300. doi: 10.32615/ps.2019.147. DOI

Ou C., Cheng W., Wang Z., Yao X., Yang S. Exogenous melatonin enhances Cd stress tolerance in Platycladus orientalis seedlings by improving mineral nutrient uptake and oxidative stress. Ecotoxicol. Environ. Saf. 2023;252:114619. doi: 10.1016/j.ecoenv.2023.114619. PubMed DOI

Lhotská M., Zemanová V., Pavlíková D., Hnilička F. Changes in the photosynthetic response of lettuce exposed to toxic element multicontamination under hydroponic conditions. Photosynthetica. 2023;61:390–397. doi: 10.32615/ps.2023.034. DOI

Yang S., Zhang J., Chen L. Growth and physiological responses of Pennisetum sp. to cadmium stress under three different soils. Environ. Sci. Pollut. Res. 2021;28:14867–14881. doi: 10.1007/s11356-020-11701-3. PubMed DOI

Shafi M., Bakht J., Razuddin H.Y., Zhang G.P. Genotypic difference in the inhibition of photosynthesis and chlorophyll fluorescence by salinity and cadmium stresses in wheat. J. Plant Nutr. 2011;34:315–323. doi: 10.1080/01904167.2011.536874. DOI

Bernardini A., Salvatori E., Guerrini V., Fusaro L., Canepari S., Manes F. Effects of high Zn and Pb concentrations on Phragmites australis (Cav.) Trin. Ex. Steudel: Photosynthetic performance and metal accumulation capacity under controlled conditions. Int. J. Phytoremediation. 2016;18:16–24. doi: 10.1080/15226514.2015.1058327. PubMed DOI

Yang Y., Zhang L., Huang X., Zhou Y., Quan Q., Li Y., Zhu X. Response of photosynthesis to different concentrations of heavy metals in Davidia involucrata. PLoS ONE. 2020;15:e0228563. doi: 10.1371/journal.pone.0228563. PubMed DOI PMC

He J., Ren Y. Effects of cadmium on seedling growth and photosynthesis characteristics of lettuce (Lactuca sativa L.) Southwest China J. Agric. Sci. 2009;22:922–926.

Cheng S., Tam N.F.Y., Li R., Shen X., Niu Z., Chai M., Qiu G.Y. Temporal variations in physiological responses of Kandelia obovata seedlings exposed to multiple heavy metals. Mar. Pollut. Bull. 2017;124:1089–1095. doi: 10.1016/j.marpolbul.2017.03.060. PubMed DOI

Liang L., Li X., Li H., Peng X., Zhang R., Tang W., Dong Y., Tang Y. Intercropping affects the physiology and cadmium absorption of pakchoi, lettuce, and radish seedlings. Environ. Sci. Pollut. Res. 2023;30:4744–4753. doi: 10.1007/s11356-022-22381-6. PubMed DOI

Chandra R., Kang H. Mixed heavy metal stress on photosynthesis, transpiration rate, and chlorophyll content in poplar hybrids. For. Sci. Technol. 2016;12:55–61. doi: 10.1080/21580103.2015.1044024. DOI

Alamer K.H., Galal T.M. Safety assessment and sustainability of consuming eggplant (Solanum melongena L.) grown in wastewater-contaminated agricultural soils. Sci. Rep. 2022;12:9768. doi: 10.1038/s41598-022-13992-7. PubMed DOI PMC

Zhang H., Li X., Xu Z., Wang Y., Teng Z., An M., Zhang Y., Zhu W., Xu N., Sun G. Toxic effects of heavy metals Pb and Cd on mulberry (Morus alba L.) seedling leaves: Photosynthetic function and reactive oxygen species (ROS) metabolism responses. Ecotoxicol. Environ. Saf. 2020;195:110469. doi: 10.1016/j.ecoenv.2020.110469. PubMed DOI

Dahlawi S., Sadiq M., Sabir M., Farooqi Z.U.R., Saifullah, Qadir A.A., Faraj T.K. Differential response of Brassica cultivars to potentially toxic elements and their distribution in different plant parts irrigated with metal-contaminated water. Sustainability. 2023;15:1966. doi: 10.3390/su15031966. DOI

Zemanová V., Pavlík M., Pavlíková D. Cadmium toxicity induced contrasting patterns of concentrations of free sarcosine, specific amino acids and selected microelements in two Noccaea species. PLoS ONE. 2017;12:e0177963. doi: 10.1371/journal.pone.0177963. PubMed DOI PMC

Xu Q., Qiu W., Lin T., Yang Y., Jiang Y. Cadmium tolerance in Elodea canadensis Michx: Subcellular distribution and metabolomic analysis. Ecotoxicol. Environ. Saf. 2023;256:114905. doi: 10.1016/j.ecoenv.2023.114905. PubMed DOI

Okunev R.V. Free amino acid accumulation in soil and tomato plants (Solanum lycopersicum L.) associated with arsenic stress. Water Air Soil Pollut. 2019;230:253. doi: 10.1007/s11270-019-4309-4. DOI

Pavlíková D., Zemanová V., Pavlík M. Health risk and quality assessment of vegetables cultivated on soils from a heavily polluted old mining area. Toxics. 2023;11:583. doi: 10.3390/toxics11070583. PubMed DOI PMC

Zhu G., Xiao H., Guo Q., Zhang Z., Zhao J., Yang D. Effects of cadmium stress on growth and amino acid metabolism in two Compositae plants. Ecotoxicol. Environ. Saf. 2018;158:300–308. doi: 10.1016/j.ecoenv.2018.04.045. PubMed DOI

Zemanová V., Pavlík M., Pavlíková D., Tlustoš P. The changes of contents of selected free amino acids associated with cadmium stress in Noccaea caerulescens and Arabidopsis halleri. Plant Soil Environ. 2013;59:417–422. doi: 10.17221/403/2013-PSE. DOI

Wan S.J., Si H.R., Wang X.Z., Chao L., Ma W., Sun S.S., Tang B., Tan X.L., Wang S. Regulation of Vicia faba L. response and its effect on Megoura crassicauda reproduction under zinc stress. Int. J. Mol. Sci. 2023;24:9659. doi: 10.3390/ijms24119659. PubMed DOI PMC

Pavlíková D., Zemanová V., Pavlík M. The contents of free amino acids and elements in As-hyperaccumulator Pteris cretica and non-hyperaccumulator Pteris straminea during reversible senescence. Plant Soil Environ. 2017;63:455–460. doi: 10.17221/606/2017-PSE. DOI

Krämer U., Cotter-Howells J.D., Charnock J.M., Baker A.J., Smith J.A.C. Free histidine as a metal chelator in plants that accumulate nickel. Nature. 1996;379:635–638. doi: 10.1038/379635a0. DOI

Pavlíková D., Pavlík M., Staszková L., Motyka V., Száková J., Tlustoš P., Balík J. Glutamate kinase as a potential biomarker of heavy metal stress in plants. Ecotoxicol. Environ. Saf. 2008;70:223–230. doi: 10.1016/j.ecoenv.2007.07.006. PubMed DOI

Majumdar R., Barchi B., Turlapati S.A., Gagne M., Minocha R., Long S., Minocha S.C. Glutamate, ornithine, arginine, proline, and polyamine metabolic interactions: The pathway is regulated at the post-transcriptional level. Front. Plant Sci. 2016;7:78. doi: 10.3389/fpls.2016.00078. PubMed DOI PMC

Deng L., Yang X., Qiu Y., Luo J., Wu H., Liu X., Zhao G., Gong H., Zheng X., Li J. Metabolic and molecular mechanisms underlying the foliar Zn application induced increase of 2-acetyl-1-pyrroline conferring the ‘taro-like’ aroma in pumpkin leaves. Front. Plant Sci. 2023;14:1127032. doi: 10.3389/fpls.2023.1127032. PubMed DOI PMC

Zhang Y., He S., Zhang Z., Xu H., Wang J., Chen H., Liu Y., Wang X., Li Y. Glycine transformation induces repartition of cadmium and lead in soil constituents. Environ. Pollut. 2019;251:930–937. doi: 10.1016/j.envpol.2019.04.099. PubMed DOI

Zemanová V., Pavlík M., Pavlíková D., Tlustoš P. The significance of methionine, histidine and tryptophan in plant responses and adaptation to cadmium stress. Plant Soil Environ. 2014;60:426–432. doi: 10.17221/544/2014-PSE. DOI

Lux A., Lackovič A., van Staden J., Lišková D., Kohanová J., Martinka M. Cadmium translocation by contractile roots differs from that in regular, non-contractile roots. Ann. Bot. 2015;115:1149–1154. doi: 10.1093/aob/mcv051. PubMed DOI PMC

Lentini M., De Lillo A., Paradisone V., Liberti D., Landi S., Esposito S. Early responses to cadmium exposure in barley plants: Effects on biometric and physiological parameters. Acta Physiol. Plant. 2018;40:178. doi: 10.1007/s11738-018-2752-2. DOI

He S., Yang X., He Z., Baligar V.C. Morphological and physiological responses of plants to cadmium toxicity: A review. Pedosphere. 2017;27:421–438. doi: 10.1016/S1002-0160(17)60339-4. 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

Duan C., Wang Y., Wang Q., Ju W., Zhang Z., Cui Y., Yuan J., Fan Q., Wei S., Li S., et al. Microbial metabolic limitation of rhizosphere under heavy metal stress: Evidence from soil ecoenzymatic stoichiometry. Environ. Pollut. 2022;300:118978. doi: 10.1016/j.envpol.2022.118978. PubMed DOI

Zemanová V., Pavlíková D., Novák M., Dobrev P.I., Matoušek T., Motyka V., Pavlík M. Arsenic-induced response in roots of arsenic-hyperaccumulator fern and soil enzymatic activity changes. Plant Soil Environ. 2022;68:213–222. doi: 10.17221/65/2022-PSE. DOI

Wahsha M., Nadimi-Goki M., Fornasier F., Al-Jawasehr R., Hussein E.I., Bini C. Microbial enzymes as an early warning management tool for monitoring mining site soils. Catena. 2017;148:40–45. doi: 10.1016/j.catena.2016.02.021. DOI

Aponte H., Meli P., Butler B., Paolini J., Matus F., Merino C., Cornejo P., Kuzyakov Y. Meta-analysis of heavy metal effects on soil enzyme activities. Sci. Total Environ. 2020;737:139744. doi: 10.1016/j.scitotenv.2020.139744. PubMed DOI

Ciadamidaro L., Madejón P., Madejón E. Soil chemical and biochemical properties under Populus alba growing: Three years study in trace element contaminated soils. Appl. Soil Ecol. 2014;73:26–33. doi: 10.1016/j.apsoil.2013.08.003. DOI

Maurya S., Abraham J.S., Somasundaram S., Toteja R., Gupta R., Makhija S. Indicators for assessment of soil quality: A mini-review. Environ. Monit. Assess. 2020;192:604. doi: 10.1007/s10661-020-08556-z. PubMed DOI

Spohn M., Kuzyakov Y. Distribution of microbial- and root-derived phosphatase activities in the rhizosphere depending on P availability and C allocation—Coupling soil zymography with 14C imaging. Soil Biol. Biochem. 2013;67:106–113. doi: 10.1016/j.soilbio.2013.08.015. DOI

Aponte H., Medina J., Butler B., Meier S., Cornejo P., Kuzyakov Y. Soil quality indices for metal(loid) contamination: An enzymatic perspective. Land Degrad. Dev. 2020;31:2700–2719. doi: 10.1002/ldr.3630. DOI

Šichorová K., Tlustoš P., Száková J., Kořínek K., Balík J. Horizontal and vertical variability of heavy metals in the soil of a polluted area. Plant Soil Environ. 2004;50:525–534. doi: 10.17221/4069-PSE. DOI

Vaněk A., Ettler V., Grygar T., Borůvka L., Šebek O., Drábek O. Combined chemical and mineralogical evidence for heavy metal binding in mining-and smelting-affected alluvial soils. Pedosphere. 2008;18:464–478. doi: 10.1016/S1002-0160(08)60037-5. DOI

Czech Ministry of the Environment . Public Notice No. 153/2016 for the Management of Soil Protection. Czech Ministry of the Environment; Prague, Czech Republic: 2016.

Břendová K., Zemanová V., Pavlíková D., Tlustoš P. Utilization of biochar and activated carbon to reduce Cd, Pb and Zn phytoavailability and phytotoxicity for plants. J. Environ. Manag. 2016;181:637–645. doi: 10.1016/j.jenvman.2016.06.042. PubMed DOI

Pavlíková D., Pavlík M., Zemanová V., Novák M., Doležal P., Dobrev P.I., Motyka V., Kraus K. Accumulation of toxic arsenic by cherry radish tuber (Raphanus sativus var. sativus Pers.) and its physiological, metabolic and anatomical stress responses. Plants. 2023;12:1257. doi: 10.3390/plants12061257. PubMed DOI PMC

Lhotská M., Zemanová V., Pavlík M., Pavlíková D., Hnilička F., Popov M. Leaf fitness and stress response after the application of contaminated soil dust particulate matter. Sci. Rep. 2022;12:10046. doi: 10.1038/s41598-022-13931-6. PubMed DOI PMC

Wellburn A.R. The spectral determination of chlorophyll a and chlorophyll b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 1994;144:307–313. doi: 10.1016/S0176-1617(11)81192-2. DOI

Porra R.J., Thompson W.A., Kriedemann P.E. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta BBA Bioenerg. 1989;975:384–394. doi: 10.1016/S0005-2728(89)80347-0. DOI

Hanč A., Dume B., Hrebečková T. Differences of enzymatic activity during composting and vermicomposting of sewage sludge mixed with straw pellets. Front. Microbiol. 2022;12:801107. doi: 10.3389/fmicb.2021.801107. PubMed DOI PMC

Novák M., Zemanová V., Pavlík M., Procházková S., Pavlíková D. Change in β-glucosidase activity in root zone of ferns under toxic elements soil contamination. Plant Soil Environ. 2023;69:124–130. doi: 10.17221/448/2022-PSE. DOI

Phytohormone and Amino Acid Changes in Cherry Radish as Metabolic Adaptive Response to Arsenic Single and Multi-Contamination