Abstract
Parsley (Petroselinum crispum) is herb with many biological and medicinal benefits for humans. However, growth on zinc (Zn) and cadmium (Cd) contaminated sites might get severely affected due to over accumulation of heavy metals (HM) in different plant tissues. Antioxidants play a crucial role in minimizing the negative effects of HM. The present study investigates the effects of Zn and Cd stress on P. crispum morphological parameters, enzymatic/non-enzymatic antioxidant profiling and metal accumulation in shoot/root. Plants were exposed to different concentrations of Zn (50, 100, 150 and 200 µM) and Cd (10, 20, 40 and 80 µM) along with control (no stress), in soil-less Hoagland's solution. The results showed that Zn and Cd substantially decrease the growth parameters with increased contents of malondialdehyde (MDA), hydrogen peroxide (H2O2), and electrolyte leakage (EL). Non-enzymatic antioxidant activities, like total phenolic contents (TPC) and ferric reducing antioxidant power (FRAP), were induced high in leaves only upon Cd stress and contrarily decreased upon Zn stress. Total flavonoid contents (TFC) were decreased under Zn and Cd stress. Enzymatic antioxidant activities like superoxide dismutase (SOD), catalase (CAT) and ascorbate peroxidase (APX) were also strongly induced upon Cd stress. At the same time, SOD and guaiacol peroxidase (GPX) activity was induced significantly upon Zn stress. Cd uptake and accumulation was notably high in roots as compared to shoots, which suggests P. crispum have a reduced ability to translocate Cd towards aboveground parts (leaves). Additionally, strong induction of antioxidants by P. crispum under Cd stress might indicate the capacity to effectively re-modulate its physiological response. However, further investigations regarding other HMs and experiments at the molecular level are still needed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abnosi M, Amirjani M, Mahdiyeh M, Moradipoor H (2015) Biochemical and cellular response of catharanthus roseus callus cells to cadmium toxicity. J Genet Resource 1:101–114. https://doi.org/10.22080/jgr.2015.1169
Ahmad A, Hadi F, Ali N (2015) 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. Int J Phytoremediation 17:56–65. https://doi.org/10.1080/15226514.2013.828018
Ahmad Z, Khan SM, Page SE, Balzter H, Ullah A, Ali S et al (2023) Environmental sustainability and resilience in a polluted ecosystem via phytoremediation of heavy metals and plant physiological adaptations. J Clean Prod 385:135733. https://doi.org/10.1016/j.jclepro.2022.135733
Al Khateeb W, Al-Qwasemeh H (2014) Cadmium, copper and zinc toxicity effects on growth, proline content and genetic stability of Solanum nigrum L., a crop wild relative for tomato; comparative study. Physiol Mol Biol Plants 20(1):31–39. https://doi.org/10.1007/s12298-013-0211-5
Alamer K, Fayez K (2020) Impact of salicylic acid on the growth and physiological activities of parsley plants under lead toxicity. Physiol Mol Biol Plants 26:1361–1373. https://doi.org/10.1007/s12298-020-00830-1
Ali H, Khan E (2019) Trophic transfer, bioaccumulation, and biomagnification of non-essential hazardous heavy metals and metalloids in food chains/webs-concepts and implications for wildlife and human health. Hum Ecol Risk Assess: Intl J 25(6):1353–1376. https://doi.org/10.1080/10807039.2018.1469398
Ali H, Khan E, Ilahi I (2019a) Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J Chem 2019:6730305
Ali MA, Fahad S, Haider I, Ahmed N, Ahmad S, Hussain S, Arshad M (2019b) Oxidative stress and antioxidant defense in plants exposed to metal/metalloid toxicity. Reactive Oxygen, Nitrogen and Sulfur Species in Plants: Production, Metabolism, Signaling and Defense Mechanisms. Jhon Wiley & Sons Ltd. ISBN: 9781119468677. https://doi.org/10.1002/9781119468677.ch15
Alves A, Ramos A, Gonçalves M, Bernardo M, Mendes B (2013) Antioxidant activity, quality parameters and mineral content of Portuguese monofloral honeys. J Food Compost Anal 30:130–138. https://doi.org/10.1016/j.jfca.2013.02.009
Aravind P, Prasad M (2003) Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L. A free floating freshwater macrophyte. Plant Physiol Biochem 4:391–397. https://doi.org/10.1016/s0981-9428(03)00035-4
Arnon D (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta Vulgaris Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Arsenov D, Župunski M, Pajević S, Borišev M, Nikolić N, Mimica-Dukić N (2021) Health assessment of medicinal herbs, celery and parsley related to cadmium soil pollution-potentially toxic elements (ptes) accumulation, tolerance capacity and Antioxidative Response. Environ Geochem Health 43:2927–2943. https://doi.org/10.1007/s10653-020-00805-x
Cui Y, Zhao N (2011) Oxidative stress and change in plant metabolism of maize (Zea mays L.) growing in contaminated soil with elemental sulfur and toxic effect of zinc. Plant, Soil Environ 57:34–39. https://doi.org/10.17221/193/2010-pse
Dhindsa R, Plumb D, Thorpe T (1981) Leaf senescence: Correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101. https://doi.org/10.1093/jxb/32.1.93
Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. azad)1. J Exp Bot 52:1101–1109. https://doi.org/10.1093/jexbot/52.358.1101
Dobrikova A, Apostolova E, Adamakis I-DS, Hanć A, Sperdouli I, Moustakas M (2022) 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.). Plants 11(18):2407. https://doi.org/10.3390/plants11182407
Fejes S, Blazovics A, Petri G (2000) Free radical scavenging and membrane protective effects of methanol extracts from Anthriscus cerefolium L. (Hoffm.) and Petroselinum crispum (Mill.) Nym. Ex A.W. Hill Phytothe Res 14:362–365. https://doi.org/10.1002/1099-1573(200008)14:5%3C362::aid-ptr554%3E3.0.co;2-g
Fryzova R, Pohanka M, Martinkova P, Cihlarova H, Brtnicky M, Hladky J, Kynicky J (2018) Oxidative stress and heavy metals in plants. Rev Environ Contam Toxicol 245:129–156. https://doi.org/10.1007/398_2017_7. (PMID: 29032515)
Gong X, Kozi A (1989) Ascorbate peroxidase in tea leaves: Occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant Cell Physiol 30:987–998. https://doi.org/10.1093/oxfordjournals.pcp.a077844
Haida Z, Hakiman M (2019) A comprehensive review on the determination of enzymatic assay and nonenzymatic antioxidant activities. Food Sci Nutr 7:1555–1563. https://doi.org/10.1002/fsn3.1012
Haider F, Liqun C, Coulter J, Cheema S, Wu J, Zhang R, Wenjun M, Farooq M (2021) Cadmium toxicity in plants: Impacts and remediation strategies. Ecotoxicol Environ Saf 211:111887. https://doi.org/10.1016/j.ecoenv.2020.111887
Hassan MJ, Raza MA, ur Rehman S, Ansar M, Gitari H, Khan I, Wajid M, Ahmed M, Shah GA, Peng Y, Li Z (2020) Effect of cadmium toxicity on growth, oxidative damage, antioxidant defense system and cadmium accumulation in two sorghum cultivars. Plants 9:1575. https://doi.org/10.3390/plants9111575
Hayes J (1986) Purification and physical characterization of glutathione s-transferase K. differential use of s-hexylglutathione and glutathione affinity matrices to isolate a novel glutathione s-transferase from rat liver. Biochem J 233:789–798. https://doi.org/10.1042/bj2330789
Hazra B, Biswas S, Mandal N (2008) Antioxidant and free radical scavenging activity of Spondias pinnata. BMC Complement Altern Med. https://doi.org/10.1186/1472-6882-8-63
Hniličková H, Hnilička F, Orsák M, Hejnák V (2019) Effect of salt stress on growth, electrolyte leakage, Na+ and K+ content in selected plant species. Plant, Soil Environ 65:90–96. https://doi.org/10.17221/620/2018-pse
Hossain MA, Piyatida P, Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:1–37
Jouad H, Haloui M, Rhiouani H, Hilaly J, Eddouks M (2001) Ethnobotanical survey of medicinal plants used for the treatment of diabetes, cardiac and renal diseases in the North Centre region of Morocco (fez-boulemane). J Ethnopharmacol 77:175–182. https://doi.org/10.1016/s0378-8741(01)00289-6
Kabata-Pendias A (2011) Trace Elements in Soils and Plants. CRC Press, Boca-Raton, FL. https://doi.org/10.1201/b10158
Khan AHA, Nawaz I, Qu Z, Butt TA, Yousaf S, Iqbal M (2020) Reduced growth response of ornamental plant Nicotiana alata L. upon selected heavy metals uptake, with co-application of ethylenediaminetetraacetic acid. Chemosphere 241:125006. https://doi.org/10.1016/j.chemosphere.2019.125006
Krippner J, Schubert S (2021) Elevated zinc concentrations did not induce thiols in spinach (Spinacia oleracea ) and parsley (Petroselinum crispum ). J Plant Nutr Soil Sci 184:439–447. https://doi.org/10.1002/jpln.202000537
Lichtenthaler H (1987) [34] chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Meth Enzymol. https://doi.org/10.1016/0076-6879(87)48036-1
Lin L, Cui C, Wen L, Yang B, Luo W, Zhao M (2011) Assessment of in vitro antioxidant capacity of stem and leaf extracts of Rabdosia serra (maxim.) Hara and identification of the major compound. Food Chem 126:54–59. https://doi.org/10.1016/j.foodchem.2010.10.060
Maehly A (2006) The assay of catalases and peroxidases. Meth Biochem Anal. https://doi.org/10.1002/9780470110171.ch14
Manivasagaperumal R, Balamurugan S, Thiyagarajan G, Sekar J (2011) Effect of zinc on germination, seedling growth and biochemical content of cluster bean (Cyamopsis tetragonoloba (L.) taub). Curr Bot 2:11–15
Manquián K, Escudey M, Zúñiga G, Arancibia M, Molina M, Cruces E (2016) Effect of cadmium on phenolic compounds, antioxidant enzyme activity and oxidative stress in blueberry (Vaccinium corymbosum L.) plantlets grown in vitro. Ecotoxicol Environ Saf 133:316–326. https://doi.org/10.1016/j.ecoenv.2016.07.029
Márquez B, Fernández R, Córdoba F (2012) Effects of cadmium on phenolic composition and antioxidant activities of Erica Andevalensis. J Bot 2012:1–6. https://doi.org/10.1155/2012/936950
Nawaz I, Iqbal M, Bliek M, Schat H (2017) Salt and heavy metal tolerance and expression levels of candidate tolerance genes among four extremophile cochlearia species with contrasting habitat preferences. Sci Total Environ 584–585:731–741. https://doi.org/10.1016/j.scitotenv.2017.01.111
Nielsen S, Young J, Daneshvar B, Lauridsen S, Knuthsen P, Sandström B, Dragsted L (1999) Effect of parsley (Petroselinum crispum) intake on urinary apigenin excretion, blood antioxidant enzymes and biomarkers for oxidative stress in human subjects. Br J Nutr 81:447–455. https://doi.org/10.1017/s000711459900080x
Pant PP, Tripathi A (2014) Impact of heavy metals on morphological and biochemical parameters of Shorea robusta plant. Ekológia 33:116. https://doi.org/10.2478/eko2014-0012
Prasad K, Saradhi PP, Sharmila P (1999) Concerted action of antioxidant enzymes and curtailed growth under zinc toxicity in Brassica juncea. Environ Exp Bot 42:1–10. https://doi.org/10.1016/S0098-8472(99)00013-1
Rizwan M, Ali S, Adrees M, Ibrahim M, Tsang D, Zia R, Zahir M, Rinklebe J, Tack F, Ok Y (2017) A critical review on effects, tolerance mechanisms and management of cadmium in vegetables. Chemosphere 182:90–105. https://doi.org/10.1016/j.chemosphere.2017.05.013
Romero-Puertas M, Rodrıguez-Serrano M, Corpas F, Gomez MD, Del Rio L, Sandalio L (2004) Cadmium-induced subcellular accumulation of O2·-and H2O2 in pea leaves. Plant Cell Environ 27:1122–1134. https://doi.org/10.1111/j.1365-3040.2004.01217.x
Saleem HM, Usman K, Rizwan M, Al Jabri H, Alsafran M (2022) Functions and strategies for enhancing zinc availability in plants for sustainable agriculture. Front Plant Sci 13:1033092. https://doi.org/10.3389/fpls.2022.1033092
Szopiński M, Sitko K, Gieroń Ż, Rusinowski S, Corso M, Hermans C, Verbruggen N, Małkowski E (2019) Toxic effects of Cd and Zn on the photosynthetic apparatus of the Arabidopsis halleri and Arabidopsis arenosa pseudo-metallophytes. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00748
Ulusu Y, Öztürk L, Elmastaş M (2017) Antioxidant capacity and cadmium accumulation in parsley seedlings exposed to cadmium stress. Russ J Plant Physiol 64:883–888. https://doi.org/10.1134/s1021443717060139
Upadhyaya A, Sankhla D, Davis T, Sankhla N, Smith B (1985) Effect of paclobutrazol on the activities of some enzymes of activated oxygen metabolism and lipid peroxidation in senescing soybean leaves. J Plant Physiol 121:453–461. https://doi.org/10.1016/s0176-1617(85)80081-x
Van AF, Cardinaels C, Clijsters H (1988) Induction of enzyme capacity in plants as a result of heavy metal toxicity: dose-response relations in Phaseolus vulgaris l., treated with zinc and cadmium. Environ Pollut 52:103–115. https://doi.org/10.1016/0269-7491(88)90084-X
Venkatachalam P, Priyanka N, Manikandan K, Ganeshbabu I, Indiraarulselvi P, Geetha MK, Bhattacharya R, Tiwari M, Sharma N, Sahi S (2017) Enhanced plant growth promoting role of phycomolecules coated zinc oxide nanoparticles with P supplementation in Cotton (Gossypium hirsutum L.). Plant Physiol Biochem 110:118–127. https://doi.org/10.1016/j.plaphy.2016.09.004
Wang C, Zhang S, Wang P, Hou J, Zhang W, Li W, Lin Z (2009) The effect of excess Zn on mineral nutrition and antioxidative response in rapeseed seedlings. Chemosphere 75:1468–1476. https://doi.org/10.1016/j.chemosphere.2009.02.033
Yang F, Zhang H, Wang Y, He G, Wang J, Guo D, Li T, Sun G, Zhang H (2021) The role of antioxidant mechanism in photosynthesis under heavy metals Cd or Zn exposure in tobacco leaves. J Plant Interact 16(1):354–366. https://doi.org/10.1080/17429145.2021.1961886
Zhai Q, Narbad A, Chen W (2015) Dietary strategies for the treatment of cadmium and lead toxicity. Nutrients 7:552–571. https://doi.org/10.3390/nu7010552
Zhang H, Chen F, Wang X, Yao H (2006) Evaluation of antioxidant activity of parsley (Petroselinum crispum) essential oil and identification of its antioxidant constituents. Food Res Int 39:833–839. https://doi.org/10.1016/j.foodres.2006.03.007
Zhang F, Wang Y, Lou Z, Dong J (2007) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67:44–50. https://doi.org/10.1016/j.chemosphere.2006.10.007
Acknowledgements
Authors are thankful to the Department of Biotechnology, COMSATS University Islamabad, Abbottabad Campus for providing faculties required for this research experiment. We are also thankful for Ms. Aimen Nasir for reference setting of the article. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. In the end, no financial disclosures or conflicts of interest is declared by authors.
Funding
This work has not received any specific funding.
Author information
Authors and Affiliations
Contributions
Conceptualization, I. N., A.M.; methodology, A.M., A.H.A.K., T.A.N.; software, A.H.A.K., R.B.; formal analysis, W.K., N.B., S.A.; investigation, I.S., K.U., S.A.; resources, T.A.N., M.M.S., I.N.; data curation, A.H.A.K., I.N.; writing-original draft preparation, review, and editing, W.K., A.H.A.K., I.N.; supervision, I.N. and M.M.S.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Nawaz, I., Mehboob, A., Khan, A.H.A. et al. Higher cadmium and zinc accumulation in parsley (Petroselinum crispum) roots activates its antioxidants defense system. Biometals 37, 87–100 (2024). https://doi.org/10.1007/s10534-023-00529-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10534-023-00529-2