{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,22]],"date-time":"2026-02-22T09:56:00Z","timestamp":1771754160542,"version":"3.50.1"},"reference-count":71,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2024,12,19]],"date-time":"2024-12-19T00:00:00Z","timestamp":1734566400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Foundation for Science and Technology (FCT)","award":["UIDB\/05748\/2020"],"award-info":[{"award-number":["UIDB\/05748\/2020"]}]},{"name":"Foundation for Science and Technology (FCT)","award":["UIDP\/05748\/2020"],"award-info":[{"award-number":["UIDP\/05748\/2020"]}]},{"name":"Foundation for Science and Technology (FCT)","award":["UIDB\/00081\/2020"],"award-info":[{"award-number":["UIDB\/00081\/2020"]}]},{"name":"Foundation for Science and Technology (FCT)","award":["UIDP\/00081\/2020"],"award-info":[{"award-number":["UIDP\/00081\/2020"]}]},{"name":"Foundation for Science and Technology (FCT)","award":["LA\/P\/0056\/2020"],"award-info":[{"award-number":["LA\/P\/0056\/2020"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Agronomy"],"abstract":"<jats:p>Metallothioneins (MTs) and phytochelatins (PCs) are small Cys-rich proteins with low molecular mass responsible for detoxifying heavy metals in cells. Arabidopsis thaliana expresses eight metallothionein genes and two types of PCS; however, there is still a need to acquire more knowledge regarding their individual responses to some heavy metals. Thus, it was intended to study the expression of AtMT- and AtPCS1-encoding genes in response to high levels of nickel in wild-type A. thaliana. Seeds of A. thaliana were placed in MS medium supplemented with increasing concentrations of Ni\u20140 mg L\u22121, 2.5 mg L\u22121, 5 mg L\u22121, 7.5 mg L\u22121, and 10 mg L\u22121. After 21 days of exposure, the expression of the AtMTs (1A, 1B, 1C, 2A, 2B, and 3) and AtPCS1 was analysed through RT-qPCR in different plant organs: roots, young leaves, and mature leaves. The concentrations of photosynthetic pigments, hydrogen peroxide, and reduced glutathione were also evaluated, but no significant changes were observed. The gene expression analysis showed that the seven genes reacted differentially to the varying concentrations of Ni and in an organ-specific way. It was noted that in roots, the expression of AtMT1A, AtMT1C, and AtMT3 increased starting with the 2.5 mg L\u22121 treatment. At the same time, the response in the leaves fluctuated more as AtMT1B and AtMT1C increased in young leaves with concentrations higher than 7.5 and 2.5 mg L\u22121, respectively, with the remaining genes analysed having their expressions decreased starting with 7.5 mg L\u22121 of Ni. In mature leaves, AtMT1A increased, while AtMT2A, AtMT2B, and AtPCS1 decreased with Ni concentrations starting from 7.5 mg L\u22121. These results strongly suggest that the increase in the expression of AtMT1B, AtMT1C, and AtMT3 in the roots significantly reduced Ni toxicity, contributing to its local accumulation and buffering its translocation to the shoots. The overall reduction in the expression of MTs and PCS1 in leaves may be linked to the active participation of MT1A in mature leaves, while young leaves depended on the increased production of MT1B and MT1C to deal with the high amount of Ni present therein. These results contribute further knowledge to the understanding of the defence mechanisms of plants against high levels of Ni regarding the participation of MTs and PCS1.<\/jats:p>","DOI":"10.3390\/agronomy14123026","type":"journal-article","created":{"date-parts":[[2024,12,19]],"date-time":"2024-12-19T03:59:43Z","timestamp":1734580783000},"page":"3026","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Nickel-Induced Differential Expression of Metallothioneins and Phytochelatin Synthase 1 in Arabidopsis thaliana: Organ-Specific Responses"],"prefix":"10.3390","volume":"14","author":[{"given":"Ana","family":"Afonseca","sequence":"first","affiliation":[{"name":"GreenUPorto\u2014Centro de Investiga\u00e7\u00e3o em Produ\u00e7\u00e3o Agroalimentar Sustent\u00e1vel\u2014Inov4Agro & Departamento de Biologia, Faculdade de Ci\u00eancias, Universidade do Porto, 4169-007 Porto, Portugal"}]},{"given":"In\u00eas","family":"Mota","sequence":"additional","affiliation":[{"name":"GreenUPorto\u2014Centro de Investiga\u00e7\u00e3o em Produ\u00e7\u00e3o Agroalimentar Sustent\u00e1vel\u2014Inov4Agro & Departamento de Biologia, Faculdade de Ci\u00eancias, Universidade do Porto, 4169-007 Porto, Portugal"}]},{"given":"Gon\u00e7alo","family":"Vasques","sequence":"additional","affiliation":[{"name":"GreenUPorto\u2014Centro de Investiga\u00e7\u00e3o em Produ\u00e7\u00e3o Agroalimentar Sustent\u00e1vel\u2014Inov4Agro & Departamento de Biologia, Faculdade de Ci\u00eancias, Universidade do Porto, 4169-007 Porto, Portugal"}]},{"given":"Leonel","family":"Soares","sequence":"additional","affiliation":[{"name":"GreenUPorto\u2014Centro de Investiga\u00e7\u00e3o em Produ\u00e7\u00e3o Agroalimentar Sustent\u00e1vel\u2014Inov4Agro & Departamento de Biologia, Faculdade de Ci\u00eancias, Universidade do Porto, 4169-007 Porto, Portugal"}]},{"given":"Mafalda","family":"Flores","sequence":"additional","affiliation":[{"name":"Departamento de Qu\u00edmica e Bioqu\u00edmica, Faculdade de Ci\u00eancias, Universidade do Porto, Rua do Campo Alegre s\/n, 4169-007 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3709-7478","authenticated-orcid":false,"given":"Manuel","family":"Azenha","sequence":"additional","affiliation":[{"name":"CIQ-UP\u2014Research Center in Chemistry, Departamento de Qu\u00edmica e Bioqu\u00edmica, Faculdade de Ci\u00eancias, Universidade do Porto, Rua do Campo Alegre s\/n, 4169-007 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2631-2112","authenticated-orcid":false,"given":"Jorge","family":"Teixeira","sequence":"additional","affiliation":[{"name":"GreenUPorto\u2014Centro de Investiga\u00e7\u00e3o em Produ\u00e7\u00e3o Agroalimentar Sustent\u00e1vel\u2014Inov4Agro & Departamento de Biologia, Faculdade de Ci\u00eancias, Universidade do Porto, 4169-007 Porto, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2024,12,19]]},"reference":[{"key":"ref_1","first-page":"1","article-title":"Halophyte quinoa: A potential hyperaccumulator of heavy metals for phytoremediation","volume":"4","author":"Ghous","year":"2022","journal-title":"Asian. J. Agric. Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"29927","DOI":"10.1007\/s11356-020-09354-3","article-title":"Toxic heavy metals: Impact on the environment and human health, and treatment with conducting organic polymers, a review","volume":"27","author":"Sall","year":"2020","journal-title":"Environ. Sci. Pollut. Res. Int."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Alengebawy, A., Abdelkhalek, S.T., Qureshi, S.R., and Wang, M.Q. (2021). Heavy Metals and Pesticides Toxicity in Agricultural Soil and Plants: Ecological Risks and Human Health Implications. Toxics, 9.","DOI":"10.3390\/toxics9030042"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"112888","DOI":"10.1016\/j.ecoenv.2021.112888","article-title":"Current trends and future prospective in nanoremediation of heavy metals contaminated soils: A way forward towards sustainable agriculture","volume":"227","author":"Ahmed","year":"2021","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1007\/s10553-020-01149-z","article-title":"Effect of Heavy Metals on Ecosystems","volume":"56","author":"Tumanyan","year":"2020","journal-title":"Chem. Technol. Fuels Oils"},{"key":"ref_6","first-page":"880","article-title":"Effect of heavy metals: An overview","volume":"51","author":"Kiran","year":"2022","journal-title":"Mater. Today: Proc."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"30","DOI":"10.18047\/poljo.26.2.4","article-title":"The remediation of agricultural land contaminated by heavy metals","volume":"26","author":"Radocaj","year":"2020","journal-title":"Poljoprivreda"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Singh, A., Prasad, S.M., and Singh, R.P. (2016). Impact of Heavy Metals on Physiological Processes of Plants: With Special Reference to Photosynthetic System. Plant Responses to Xenobiotics, Springer.","DOI":"10.1007\/978-981-10-2860-1"},{"key":"ref_9","first-page":"1612","article-title":"Heavy metals and its impact in vegetable crops","volume":"7","author":"Sandeep","year":"2018","journal-title":"Int. J. Chem. Stud."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"112336","DOI":"10.1016\/j.ecoenv.2021.112336","article-title":"Impacts of heavy metals and medicinal crops on ecological systems, environmental pollution, cultivation, and production processes in China","volume":"219","author":"Chen","year":"2021","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"12673","DOI":"10.1007\/s11356-019-04892-x","article-title":"Nickel toxicity in plants: Reasons, toxic effects, tolerance mechanisms, and remediation possibilities\u2014A review","volume":"26","author":"Hassan","year":"2019","journal-title":"Environ. Sci. Pollut. Res. Int."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"16860","DOI":"10.1007\/s11356-021-18419-w","article-title":"Heavy metal\u2013induced stress in eukaryotic algae\u2014Mechanisms of heavy metal toxicity and tolerance with particular emphasis on oxidative stress in exposed cells and the role of antioxidant response","volume":"29","author":"Nowicka","year":"2022","journal-title":"Environ. Sci. Pollut. Res. Int."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Buxton, S., Garman, E., Heim, K.E., Lyons-Darden, T., Schlekat, C.E., Taylor, M.D., and Oller, A.R. (2019). Concise Review of Nickel Human Health Toxicology and Ecotoxicology. Inorganics, 7.","DOI":"10.3390\/inorganics7070089"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"111175","DOI":"10.1016\/j.ecoenv.2020.111175","article-title":"Copper and zinc differentially affect root glutathione accumulation and phytochelatin synthase gene expression of Rhizophora mucronata seedlings: Implications for mechanisms underlying trace metal tolerance","volume":"205","author":"Phongdara","year":"2020","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1080\/13102818.2018.1559096","article-title":"Comparative analyses of phytochelatin synthase (PCS) genes in higher plants","volume":"33","author":"Filiz","year":"2019","journal-title":"Biotechnol. Biotechnol. Equip."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1016\/j.plaphy.2006.10.021","article-title":"Leaf-targeted phytochelatin synthase in Arabidopsis thaliana","volume":"44","author":"Peterson","year":"2006","journal-title":"Plant Physiol. Biochem."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2665","DOI":"10.1007\/s12298-021-01103-1","article-title":"Over-expression of chickpea metallothionein 1 gene confers tolerance against major toxic heavy metal stress in Arabidopsis","volume":"27","author":"Dubey","year":"2021","journal-title":"Physiol. Mol. Biol. Plants"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"3575","DOI":"10.1093\/jxb\/erl102","article-title":"Expression of BjMT2, a metallothionein 2 from Brassica juncea, increases copper and cadmium tolerance in Escherichia coli and Arabidopsis thaliana, but inhibits root elongation in Arabidopsis thaliana seedlings","volume":"57","author":"Zhigang","year":"2006","journal-title":"J. Exp. Bot."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1247","DOI":"10.1007\/s00425-018-2859-0","article-title":"The rice \u201cfruit-weight 2.2-like\u201d gene family member OsFWL4 is involved in the translocation of cadmium from roots to shoots","volume":"247","author":"Xiong","year":"2018","journal-title":"Planta"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1007\/s12374-009-9076-0","article-title":"Arabidopsis thaliana Metallothionein, AtMT2a, Mediates ROS Balance during Oxidative Stress","volume":"52","author":"Zhu","year":"2009","journal-title":"J. Plant. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1007\/s12041-014-0430-8","article-title":"Expression of the rgMT gene, encoding for a rice metallothionein-like protein in Saccharomyces cerevisiae and Arabidopsis thaliana","volume":"93","author":"Jin","year":"2014","journal-title":"J. Genet."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1697","DOI":"10.1104\/pp.108.115782","article-title":"Examining the specific contributions of individual Arabidopsis metallothioneins to copper distribution and metal tolerance","volume":"146","author":"Guo","year":"2008","journal-title":"Plant Physiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/j.envexpbot.2011.02.017","article-title":"Metallothionein 1 (CcMT1) of pigeonpea (Cajanus cajan, L.) confers enhanced tolerance to copper and cadmium in Escherichia coli and Arabidopsis thaliana","volume":"72","author":"Sekhar","year":"2011","journal-title":"Environ. Exp. Bot."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1007\/s00128-014-1444-x","article-title":"The heterologous expression of the Iris lactea var. chinensis type 2 metallothionein IlMT2b gene enhances copper tolerance in Arabidopsis thaliana","volume":"94","author":"Gu","year":"2015","journal-title":"Bull. Environ. Contam. Toxicol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1046\/j.1469-8137.2003.00813.x","article-title":"Characterization of the Arabidopsis metallothionein gene family: Tissue-specific expression and induction during senescence and in response to copper","volume":"159","author":"Guo","year":"2003","journal-title":"New Phytol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/S0014-5793(01)02976-3","article-title":"Arabidopsis thaliana expresses a second functional phytochelatin synthase","volume":"507","author":"Clemens","year":"2001","journal-title":"FEBS Lett."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"22449","DOI":"10.1074\/jbc.M313142200","article-title":"Phytochelatin synthase, a dipeptidyltransferase that undergoes multisite acylation with gamma-glutamylcysteine during catalysis: Stoichiometric and site-directed mutagenic analysis of Arabidopsis thaliana PCS1-catalyzed phytochelatin synthesis","volume":"279","author":"Vatamaniuk","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.gene.2017.12.042","article-title":"Two mulberry phytochelatin synthase genes confer zinc\/cadmium tolerance and accumulation in transgenic Arabidopsis and tobacco","volume":"645","author":"Fan","year":"2018","journal-title":"Gene"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1016\/j.plaphy.2010.08.016","article-title":"Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants","volume":"48","author":"Gill","year":"2010","journal-title":"Plant Physiol. Biochem."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"135196","DOI":"10.1016\/j.chemosphere.2022.135196","article-title":"Heavy metal and metalloid toxicity in horticultural plants: Tolerance mechanism and remediation strategies","volume":"303","author":"Noor","year":"2022","journal-title":"Chemosphere"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"131957","DOI":"10.1016\/j.chemosphere.2021.131957","article-title":"Metal tolerance in plants: Molecular and physicochemical interface determines the \u201cnot so heavy effect\u201d of heavy metals","volume":"287","author":"Thakur","year":"2022","journal-title":"Chemosphere"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Hasanuzzaman, M., and Fujita, M. (2022). Plant Oxidative Stress: Biology, Physiology and Mitigation. Plants, 11.","DOI":"10.3390\/plants11091185"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1074","DOI":"10.1007\/s00128-022-03535-1","article-title":"The Effect of Nickel Exposure on Oxidative Stress of Vicia faba Plants","volume":"108","author":"Helaoui","year":"2022","journal-title":"Bull. Environ. Contam. Toxicol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.molp.2014.12.007","article-title":"Carotenoid Metabolism in Plants","volume":"8","author":"Nisar","year":"2015","journal-title":"Mol. Plant"},{"key":"ref_35","first-page":"424","article-title":"The role of oxidative stress on carotene production by Blakeslea trispora in submerged fermentation","volume":"36","author":"Roukas","year":"2016","journal-title":"Crit. Rev. Biotechnol."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Hasanuzzaman, M., Bhuyan, M., Anee, T.I., Parvin, K., Nahar, K., Mahmud, J.A., and Fujita, M. (2019). Regulation of Ascorbate-Glutathione Pathway in Mitigating Oxidative Damage in Plants under Abiotic Stress. Antioxidants, 8.","DOI":"10.3390\/antiox8090384"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1337","DOI":"10.1534\/genetics.118.300755","article-title":"Biology in Bloom: A Primer on the Arabidopsis thaliana Model System","volume":"208","author":"Woodward","year":"2018","journal-title":"Genetics"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1146\/annurev.arplant.53.100301.135154","article-title":"Phytochelatins and metallothioneins: Roles in heavy metal detoxification and homeostasis","volume":"53","author":"Cobbett","year":"2002","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_39","first-page":"875","article-title":"Functional homologs of fungal metallothionein genes from Arabidopsis","volume":"6","author":"Zhou","year":"1994","journal-title":"Plant Cell"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1007\/BF02191599","article-title":"Structure, organization and expression of the metallothionein gene family in Arabidopsis","volume":"248","author":"Zhou","year":"1995","journal-title":"Mol. Genet. Genom"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3325","DOI":"10.1093\/emboj\/18.12.3325","article-title":"Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast","volume":"18","author":"Clemens","year":"1999","journal-title":"EMBO J."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"111357","DOI":"10.1016\/j.plantsci.2022.111357","article-title":"Arabidopsis SUMO E3 ligase SIZ1 enhances cadmium tolerance via the glutathione-dependent phytochelatin synthesis pathway","volume":"322","author":"Zheng","year":"2022","journal-title":"Plant Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"153011","DOI":"10.1016\/j.jplph.2019.153011","article-title":"Overexpression of phytochelatin synthase AtPCS2 enhances salt tolerance in Arabidopsis thaliana","volume":"240","author":"Kim","year":"2019","journal-title":"J. Plant Physiol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., and S\u00f6ding, J. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol., 7.","DOI":"10.1038\/msb.2011.75"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"52","DOI":"10.6026\/97320630005052","article-title":"PrimerIdent: A web based tool for conserved primer design","volume":"5","author":"Pessoa","year":"2010","journal-title":"Bioinformation"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1656","DOI":"10.1080\/09168451.2018.1486177","article-title":"Comparative expression analysis of genes encoding metallothioneins in response to heavy metals and abiotic stresses in rice (Oryza sativa) and Arabidopsis thaliana","volume":"82","author":"Kim","year":"2018","journal-title":"Biosci. Biotechnol. Biochem."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"5509","DOI":"10.1093\/jxb\/err228","article-title":"Cadmium tolerance and phytochelatin content of Arabidopsis seedlings over-expressing the phytochelatin synthase gene AtPCS1","volume":"62","author":"Brunetti","year":"2011","journal-title":"J. Exp. Bot."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Takeuchi, H., and Higashiyama, T. (2012). A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis. PLoS Biol., 10.","DOI":"10.1371\/journal.pbio.1001449"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Ferreira, M.J., Silva, J., Pinto, S.C., and Coimbra, S. (2023). I Choose You: Selecting Accurate Reference Genes for qPCR Expression Analysis in Reproductive Tissues in Arabidopsis thaliana. Biomolecules, 13.","DOI":"10.3390\/biom13030463"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1343","DOI":"10.1007\/s00425-008-0706-4","article-title":"Normalisation of real-time RT-PCR gene expression measurements in Arabidopsis thaliana exposed to increased metal concentrations","volume":"227","author":"Remans","year":"2008","journal-title":"Planta"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Alves, A., Ribeiro, R., Azenha, M., Cunha, M., and Teixeira, J. (2023). Effects of Exogenously Applied Copper in Tomato Plants\u2019 Oxidative and Nitrogen Metabolisms under Organic Farming Conditions. Horticulturae, 9.","DOI":"10.3390\/horticulturae9030323"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"109860","DOI":"10.1016\/j.scienta.2020.109860","article-title":"Assessing predawn leaf water potential based on hyperspectral data and pigment\u2019s concentration of Vitis vinifera L. in the Douro Wine Region","volume":"278","author":"Tosin","year":"2021","journal-title":"Sci. Hortic."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"100034","DOI":"10.1016\/j.stress.2021.100034","article-title":"Cr (VI)-induced oxidative damage impairs ammonia assimilation into organic forms in Solanum lycopersicum L.","volume":"2","author":"Martins","year":"2021","journal-title":"Plant Stress"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1038\/nmeth.2089","article-title":"NIH Image to ImageJ: 25 years of image analysis","volume":"9","author":"Schneider","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/S0038-0717(01)00150-X","article-title":"Fresh additions of heavy metals do not model long-term effects on microbial biomass and activity","volume":"34","author":"Renella","year":"2002","journal-title":"Soil. Biol. Biochem."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2031","DOI":"10.1016\/j.soilbio.2009.04.026","article-title":"Heavy metals and soil microbes","volume":"41","author":"Giller","year":"2009","journal-title":"Soil. Biol. Biochem."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"2592","DOI":"10.1897\/02-503","article-title":"Comparison of toxicity of zinc for soil microbial processes between laboratory-contamined and polluted field soils","volume":"22","author":"Smolders","year":"2003","journal-title":"Environ. Toxicol. Chem."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1016\/j.jplph.2010.09.009","article-title":"Soluble silicon modulates expression of Arabidopsis thaliana genes involved in copper stress","volume":"168","author":"Khandekar","year":"2011","journal-title":"J. Plant Physiol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"16040","DOI":"10.1007\/s11356-019-04972-y","article-title":"Bioaccumulation, antioxidative response, and metallothionein expression in Lupinus luteus L. exposed to heavy metals and silver nanoparticles","volume":"26","author":"Jaskulak","year":"2019","journal-title":"Environ. Sci. Pollut. Res. Int."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1046\/j.1469-8137.2002.00506.x","article-title":"Ni-induced oxidative stress in roots of the Ni hyperaccumulator, Alyssum bertolonii","volume":"156","author":"Boominathan","year":"2002","journal-title":"New Phytol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1007\/s10725-009-9386-8","article-title":"Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings","volume":"59","author":"Maheshwari","year":"2009","journal-title":"Plant Growth Regul."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1489","DOI":"10.1016\/j.jplph.2006.10.001","article-title":"Cadmium hyperaccumulation leads to an increase of glutathione rather than phytochelatins in the cadmium hyperaccumulator Sedum alfredii","volume":"164","author":"Sun","year":"2007","journal-title":"J. Plant Physiol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/S0098-8472(99)00057-X","article-title":"Stress indications in copper- and nickel-exposed Scots pine seedlings","volume":"43","author":"Kukkola","year":"2000","journal-title":"Environ. Exp. Bot."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"2176","DOI":"10.1105\/tpc.104.023036","article-title":"Increased glutathione biosynthesis plays a role in nickel tolerance in thlaspi nickel hyperaccumulators","volume":"16","author":"Freeman","year":"2004","journal-title":"Plant Cell"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1007\/s10534-006-9011-5","article-title":"Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves","volume":"20","author":"Gajewska","year":"2007","journal-title":"Biometals"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/j.jplph.2014.10.011","article-title":"Root based responses account for Psidium guajava survival at high nickel concentration","volume":"174","author":"Bazihizina","year":"2015","journal-title":"J. Plant Physiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1080\/01904160902872800","article-title":"Excess Nickel Alters Growth, Metabolism, and Translocation of Certain Nutrients in Potato","volume":"32","author":"Shukla","year":"2009","journal-title":"J. Plant Nutr."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1016\/S0168-9452(02)00210-8","article-title":"Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage","volume":"163","author":"Pandey","year":"2002","journal-title":"Plant Sci."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1963","DOI":"10.1016\/0031-9422(80)83013-5","article-title":"Nature of nickel complexes in Psychotria douarrei and other nickel-accumulating plants","volume":"19","author":"Kersten","year":"1980","journal-title":"Phytochemistry"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1503","DOI":"10.1016\/0031-9422(77)84010-7","article-title":"Isolation and identification of a citrato-complex of nickel from nickel-accumulating plants","volume":"16","author":"Lee","year":"1977","journal-title":"Phytochemistry"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1695","DOI":"10.1016\/j.phytochem.2008.02.009","article-title":"Identification of nickel chelators in three hyperaccumulating plants: An X-ray spectroscopic study","volume":"69","author":"Chardot","year":"2008","journal-title":"Phytochemistry"}],"container-title":["Agronomy"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4395\/14\/12\/3026\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:55:19Z","timestamp":1760115319000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4395\/14\/12\/3026"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,19]]},"references-count":71,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["agronomy14123026"],"URL":"https:\/\/doi.org\/10.3390\/agronomy14123026","relation":{},"ISSN":["2073-4395"],"issn-type":[{"value":"2073-4395","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,19]]}}}