Abstract
In order to assess the impact of copper (Cu) stress on plant metabolism, sunflower seedlings were cultivated for 15 days on a nutrient medium and then transferred to the same medium enriched with increasing concentrations of Cu (0, 2.5, 5, 10, 50 and 100 μM). When copper doses in the culture medium exceeded 10 µM, a reduction in biomass production, more pronounced in roots than in leaves and stems, was noticed. Excess Cu disrupted the mineral composition of the plant tissues. This effect was reflected in decreased contents of K, Mg, Zn and Mn and enhanced amounts of Fe in roots at the highest doses of Cu (50 and 100 µM). However, Ca content was not affected by Cu stress in any plant organ. These findings were further confirmed by a principal component analysis (PCA) of the mineral composition of sunflower tissues and the applied treatments. A Cu excess enhanced the accumulation of oxidative stress biomarkers in plant tissues, namely malondialdehyde and hydrogen peroxide (H2O2), testifying to the disruption of the cellular redox state. This impact was aggravated by the inhibition of antioxidative enzymes such as superoxide dismutase, catalase and ascorbate peroxidase. However, the stimulation of guaiacol peroxidase activity could be correlated with its role in membrane lignification. Based on the current findings, we suggest that the tolerance threshold of a sunflower plant to Cu stress is 10 µM. When Cu exceeds this concentration in the culture medium, toxicity symptoms may occur in the plant.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Data availability
The datasets analysed during the current study are available from the corresponding author on reasonable request.
References
Aebi H (1984) Catalase in vitro. Meth Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Barros J, Serk H, Granlund I, Pesquet E (2015) The cell biology of lignification in higher plants. Ann Bot 115:1053–1074. https://doi.org/10.1093/aob/mcv046
Ben Massoud M, Sakouhi L, Chaoui A (2019) Effect of plant growth regulators, calcium and citric acid on copper toxicity in pea seedlings. J Plant Nutr 42:1230–1242. https://doi.org/10.1080/01904167.2019.1609506
Ben Massoud M, Kharbech O, Sakouhi L et al. (2022) Calcium and citrate protect Pisum sativum roots against copper toxicity by regulating the cellular redox status. J Soil Sci Plant Nutr 22:345–358. https://doi.org/10.1007/s42729-021-00652-4
Chaffai R, Elhammadi MA, Seybou TN et al. (2007) Altered fatty acid profile of polar lipids in maize seedlings in response to excess copper. J Agron Crop Sci 193:207–217. https://doi.org/10.1111/j.1439-037X.2007.00252.x
Ferreira CSS, Seifollahi-Aghmiuni S, Destouni G et al. (2022) Soil degradation in the European Mediterranean region: processes, status and consequences. Sci Total Environ 805:150106. https://doi.org/10.1016/j.scitotenv.2021.150106
Fielding JL, Hall JL (1978) A biochemical and cytochemical study of peroxidase activity in roots of Pisum sativum: II. Distribution of enzymes in relation to root development. J Exp Bot 29:983–991. https://doi.org/10.1093/jxb/29.4.983
Ghosh S, Sarkar P, Basak P et al. (2018) Role of heat shock proteins in oxidative stress and stress tolerance. In: Asea AAA, Kaur P (eds) Heat shock proteins and stress. Springer International, Cham, pp 109–126. https://doi.org/10.1007/978-3-319-90725-3
Gomes DG, Lopes-Oliveira PJ, Debiasi TV et al. (2021) Regression models to stratify the copper toxicity responses and tolerance mechanisms of Glycine max (L.) Merr. plants. Planta 253:43. https://doi.org/10.1007/s00425-021-03573-9
Hardiman RT, Jacoby B, Banin A (1984) Factors effecting the distribution of cadmium, copper and lead and their effect upon yield and zinc content in bush beans (Phaseolus vulgaris L.). Plant Soil 81:17–27. https://doi.org/10.1007/BF02206890
Hasan MK, Ahammed GJ, Yin L et al. (2015) Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicum L. Front Plant Sci 6:601. https://doi.org/10.3389/fpls.2015.00601
Hasanuzzaman M, Bhuyan MHMB, Zulfiqar F et al. (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9:681. https://doi.org/10.3390/antiox9080681
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Hippler FWR, Boaretto RM, Dovis VL et al. (2018) Oxidative stress induced by Cu nutritional disorders in citrus depends on nitrogen and calcium availability. Sci Rep 8:1641. https://doi.org/10.1038/s41598-018-19735-x
Kharbech O, Sakouhi L, Mahjoubi Y et al. (2022) Nitric oxide donor, sodium nitroprusside modulates hydrogen sulfide metabolism and cysteine homeostasis to aid the alleviation of chromium toxicity in maize seedlings (Zea mays L.). J Hazar Mater 424:127302. https://doi.org/10.1016/j.jhazmat.2021.127302
Kosakivska IV, Babenko LM, Romanenko KO et al. (2021) Molecular mechanisms of plant adaptive responses to heavy metals stress. Cell Biol Int 45:258–272. https://doi.org/10.1002/cbin.11503
Liu J, Wang J, Lee S, Wen R (2018) Copper-caused oxidative stress triggers the activation of antioxidant enzymes via ZmMPK3 in maize leaves. PLoS ONE 13:e0203612. https://doi.org/10.1371/journal.pone.0203612
Marastoni L, Sandri M, Pii Y et al. (2019) Synergism and antagonisms between nutrients induced by copper toxicity in grapevine rootstocks: monocropping vs. intercropping. Chemosphere 214:563–578. https://doi.org/10.1016/j.chemosphere.2018.09.127
Marques DM, Veroneze Júnior V, da Silva AB et al. (2018) Copper toxicity on photosynthetic responses and root morphology of Hymenaea courbaril L. (Caesalpinioideae). Water Air Soil Pollut 229:138. https://doi.org/10.1007/s11270-018-3769-2
Migocka M, Malas K (2018) Plant responses to copper: molecular and regulatory mechanisms of copper uptake, distribution and accumulation in plants. In: Hossain MA, Kamiya T, Burritt DJ et al (eds) Plant micronutrient use efficiency. Academic, Cambridge, pp 71–86. https://doi.org/10.1016/B978-0-12-812104-7.00005-8
Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175. https://doi.org/10.1016/S0021-9258(19)45228-9
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Palm E, Guidi Nissim W, Giordano C et al. (2017) Root potassium and hydrogen flux rates as potential indicators of plant response to zinc, copper and nickel stress. Environ Experim Bot 143:38–50. https://doi.org/10.1016/j.envexpbot.2017.08.009
Rehman M, Maqbool Z, Peng D, Liu L (2019) Morpho-physiological traits, antioxidant capacity and phytoextraction of copper by ramie (Boehmeria nivea L.) grown as fodder in copper-contaminated soil. Environ Sci Pollut Res 26:5851–5861. https://doi.org/10.1007/s11356-018-4015-6
Sağlam A, Yetişsin F, Demiralay M, Terzi R (2016) Copper stress and responses in plants. In: Ahmad P (ed) Plant metal interaction. Elsevier, Amsterdam, pp 21–40. https://doi.org/10.1016/B978-0-12-803158-2.00002-3
Sakouhi L, Rahoui S, Ben Massoud M et al. (2016) Calcium and EGTA alleviate cadmium toxicity in germinating chickpea seeds. J Plant Growth Regul 35(4):1064–1073. https://doi.org/10.1007/s00344-016-9605-2
Sakouhi L, Kharbech O, Massoud MB et al. (2021) Calcium and ethylene glycol tetraacetic acid mitigate toxicity and alteration of gene expression associated with cadmium stress in chickpea (Cicer arietinum L.) shoots. Protoplasma 258:849–861. https://doi.org/10.1007/s00709-020-01605-x
Sakouhi L, Kharbech O, Ben Massoud M et al. (2022a) Oxalic acid mitigates cadmium toxicity in Cicer arietinum L. germinating seeds by maintaining the cellular redox homeostasis. J Plant Growth Regul 35:1064–1073. https://doi.org/10.1007/s00344-021-10334-1
Sakouhi L, Kharbech O, Ben Massoud M et al. (2022b) Oxalic acid protects germinating chickpea seeds against cadmium injury. J Soil Sci Plant Nutr 2:647–659. https://doi.org/10.1007/s42729-021-00675-x
Sakouhi L, Mahjoubi Y, Labben A et al. (2022c) Effects of cadmium–selenium interaction on glyoxalase and antioxidant systems of Pisum sativum germinating seeds. J Plant Growth Regul. https://doi.org/10.1007/s00344-022-10772-5
Sergiev I, Alexieva V, Karanov E (1997) Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Comt Rend Acad Bulg Sci 51:121–124
Shabbir Z, Sardar A, Shabbir A et al. (2020) Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil-plant environment. Chemosphere 259:127436. https://doi.org/10.1016/j.chemosphere.2020.127436
Shams M, Ekinci M, Turan M et al. (2019) Growth, nutrient uptake and enzyme activity response of Lettuce (Lactuca sativa L.) to excess copper. J Environ Sustain 2:67–73. https://doi.org/10.1007/s42398-019-00051-7
Su N, Ling F, Xing A et al. (2020) Lignin synthesis mediated by CCoAOMT enzymes is required for the tolerance against excess Cu in Oryza sativa. Environ Experim Bot 175:104059. https://doi.org/10.1016/j.envexpbot.2020.104059
Triantafyllidis V, Zotos A, Kosma C et al. (2020) Environmental implications from long-term citrus cultivation and wide use of Cu fungicides in Mediterranean soils. Water Air Soil Pollut 231:218. https://doi.org/10.1007/s11270-020-04577-z
Yadav P, Kaur R, Kanwar MK et al. (2018) Ameliorative role of castasterone on copper metal toxicity by improving redox homeostasis in Brassica juncea L. J Plant Growth Regul 37:575–590. https://doi.org/10.1007/s00344-017-9757-8
Funding
This work was financially supported by the Tunisian Ministry of High Education and Scientific Research (LR18ES38).
Author information
Authors and Affiliations
Contributions
LS: experiments, statistical analysis, writing—original draft; EEF: conceptualization, supervision. All authors have read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interest
All authors declare that they have no conflict of interest.
Additional information
Responsible Editor: Mohamed Ksibi.
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
Sakouhi, L., Ferjani, E.E. Effects of excess copper on sunflower seedling growth, mineral nutrition, and cellular redox state. Euro-Mediterr J Environ Integr 7, 583–591 (2022). https://doi.org/10.1007/s41207-022-00335-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s41207-022-00335-1