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Plantago lanceolata L. from Serpentine Soils in Central Bosnia Tolerates High Levels of Heavy Metals in Soil

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Abstract

Plants evolved a number of coping mechanisms wherewith they overcome negative environmental influences. Secondary metabolites are essential in plants’ stress management toolbox. One of the crucial environmental problems is contamination of soil with toxic heavy metals by different human activities. Serpentine soils are naturally burdened with heavy metals, thus presenting a great model for studying heavy metal tolerance in plants and their mechanisms of adapting to metalliferous soils. Plantago lanceolata L. is a widespread species adapted to both different environmental factors and different soils. In order to analyze the physiological status of P. lanceolata populations from metalliferous and non-metalliferous soils, we collected specimens from metalliferous soils including serpentine outcrops of central Bosnia and area artificially contaminated with heavy metals as well as from non-metalliferous soil. Heavy metal content (Cd, Cr, Mn, Co, Cu, Ni, Pb, Zn, and Fe) was determined in both herb and soil in order to test metal availability and accumulation potential of the analyzed individuals. Contents of total phenolics, phenolic acids, flavonoids, chlorophylls a and b, and proline were determined using spectrophotometric methods. The highest content of total phenolics was observed in a sample from anthropogenic site while proline showed a higher concentration in plants from serpentine soils. Regardless of high concentrations of Ni, Zn, and Cr in soil, P. lanceolata showed remarkable tolerance to serpentine soils as no significant differences in biochemical and physiological parameters were found in plants from metalliferous and non-metalliferous sites. These results indicate the existence of adaptive mechanisms and potential use of P. lanceolata in the remediation of heavy metal–polluted soils.

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References

  • Arthur, E. L., Rice, P. J., Rice, P. J., Anderson, T. A., Baladi, S. M., Henderson, K. L. D., & Coats, J. R. (2005). Phytoremediation – an overview. Critical Reviews in Plant Sciences, 24, 109–122. https://doi.org/10.1080/07352680590952496.

    Article  CAS  Google Scholar 

  • ATSDR (2008). Draft toxicological profile for manganese. U.S. Department of Health and Human Services, Public Health Service. Agency for Toxic Substances and Disease Registry, USA.

  • Baker, A. J. M. (1981). Accumulators and excluders – strategies in the response of plants to heavy –metals. Journal of Plant Nutrition, 3(1–4), 643–654. https://doi.org/10.1080/01904168109362867.

    Article  CAS  Google Scholar 

  • Bhargava, A., Carmona, F. F., Bhargava, M., & Srivastava, S. (2012). Approaches for enhanced phytoextraction of heavy metals. Journal of Environmental Management, 105, 103–120. https://doi.org/10.1016/j.jenvman.2012.04.002.

    Article  CAS  Google Scholar 

  • Carillo, P., & Gibon, Y. (2011). PROTOCOL: extraction and determination of proline. Prometheus Wiki.

  • Chaves, M. M., Costa, J. M., & Saibo, N. J. M. (2011). Recent advances in photosynthesis under drought and salinity. In I. Turkan (Ed.), Advances in botanical research (Vol. 57, pp. 50–83). https://doi.org/10.1016/B978-0-12-387692-8.00003-5.

    Chapter  Google Scholar 

  • Cook, M. E. (1994). "Cadmium pigments: when should I use them?" Inorganic pigments. Environmental issues and technological opportunities. London: Industrial Inorganic Chemicals Group, Royal Society of Chemistry.

    Google Scholar 

  • Da Silva, W. R., Da Silva, F. B. V., Araujo, P. R. M., & Do Nascimento, C. W. A. (2017). Assessing human health risks and strategies for phytoremediation in soils contaminated with As, Cd, Pb, and Zn by slag disposal. Ecotoxicology and Environmental Safety, 144, 522–530. https://doi.org/10.1016/j.ecoenv.2017.06.068.

    Article  CAS  Google Scholar 

  • Denneman, P. R. J., & Robberse, J. G. (1990). Contaminated soils “90”. In F. Arendt, M. Hinsenveld, & W. J. Vab Den Brink (Eds.), Ecotoxicological risk assessment as a base for development of soil quality criteria. Dordrecht: Kluwer.

    Chapter  Google Scholar 

  • Dixit, V., Pandey, V., & Shyam, R. (2002). Chromium ions inactivate electron transport and enhance superoxide generation in vivo in pea (Pisum sativum L. cv. Azad) root mitochondria. Plant, Cell & Environment, 25, 687–690. https://doi.org/10.1046/j.1365-3040.2002.00843.x.

    Article  CAS  Google Scholar 

  • Eddy, N. O., Odoemelam, S. A., & Mbaba, A. (2006). Elemental composition of soil in some dumpsites. Electronic Journal of Environmental, Agricultural and Food Chemistry, 5(3), 1349–1136. https://doi.org/10.4314/jasem.v18i1.1.10.

    Article  CAS  Google Scholar 

  • FAO/WHO (1976). List of maximum levels recommended for contaminants by the joint FAO/WHO codex Alimentarias Commission. 2nd series, CAC/FAL, 1976, 3: 1–8.

  • Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST: palaeontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 9.

    Google Scholar 

  • Hayat, S., Hayat, Q., Alyemeni, M. N., Wani, A. S., Pichtel, J., & Ahmad, A. (2012). Role of proline under changing environments. Plant Signaling and Behavior, 7(11), 1456–1466. https://doi.org/10.4161/psb.21949.

    Article  CAS  Google Scholar 

  • International Organization for Standardization. (1995). Soil quality – extraction of trace elements soluble in aqua regia. International Standard ISO 11466:1995. Geneve, Switzerland.

  • International Organization for Standardization. (1998). Soil quality – determination of cadmium, chromium, cobalt, copper, lead, manganese, nickel and zinc, flame and electrothermal AAS. International standard ISO 11047:1998. Geneve, Switzerland.

  • Jain, R., Srivastava, S., Madan, V. K., & Jain, R. (2000). Influence of chromium on growth and cell division of sugarcane. Indian Journal of Plant Physiology, 5, 228–231.

    CAS  Google Scholar 

  • Jaleel, C. A., Jayakumar, K., Chang-Xing, Z., & Iqbal, M. (2009). Low concentration of cobalt increases growth, biochemical constituents, mineral status and yield in Zea Mays. Journal of Scientific Research, 1(1), 128–137. https://doi.org/10.3329/jsr.vlil.1226.

    Article  Google Scholar 

  • Jayakumar, K., & Jaleel, C. A. (2009). Uptake and accumulation of cobalt in plants: a study based on exogenous cobalt in soybean. Botany Research International, 2(4), 310–314.

    CAS  Google Scholar 

  • Keilig, K., & Ludwig-Müller, J. (2009). Effect of flavonoids on heavy metal tolerance in Arabidopsis thaliana seedlings. Botanical Studies, 50, 311–318.

    CAS  Google Scholar 

  • Koptsik, G. N. (2014). Problems and prospects concerning the phytoremediation of heavy metal polluted soils: a review. Eurasian Soil Science, 47(9), 923–939. https://doi.org/10.1134/S1064229314090075.

    Article  CAS  Google Scholar 

  • Korkina, L. G. (2007). Phenylpropanoids as naturally occurring antioxidants: from plant defence to human health. Cellular and Molecular Biology, 53, 15–25. https://doi.org/10.1170/T772.

    Article  CAS  Google Scholar 

  • Kováčik, J., & Klejdus, B. (2008). Dynamics of phenolic acids and lignin accumulation in metal-treated Matricaria chamomilla roots. Plant Cell Reports, 27, 605–615. https://doi.org/10.1007/s00299-007-0490-9.

    Article  CAS  Google Scholar 

  • Kulbat, K., & Leszczyńska, J. (2015). Antioxidants as a defensive shield in thyme (Thymus vulgaris L.) grown on the soil contaminated with heavy metals. Biotechnology and Food Science, 7(2), 109–117.

    Google Scholar 

  • Lavid, N., Schwartz, A., Yarden, O., & Telor, E. (2001). The involvement of polyphenols and peroxidase activities in heavy metal accumulation by epidermal glands of waterlily (Nymphaeceaea). Planta, 212(3), 323–331. https://doi.org/10.1007/s004250000400.

    Article  CAS  Google Scholar 

  • Li, Y., Kui-Shan, W., Xiao, R., Ying-Xian, Z., Feng, W., & Qiang, W. (2018). Response of plant secondary metabolites to environmental factors. Molecules, 23(4), 762. https://doi.org/10.3390/molecules23040762.

    Article  CAS  Google Scholar 

  • Lichtenthaler, H. K. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350–382. https://doi.org/10.1016/0076-6879(87)48036-1.

    Article  CAS  Google Scholar 

  • Lisjak, M., Spoljarević, M., Agić, D., & Andrić, L. (2009). Practicum – plant physiology. Osijek: Joseph George Strossmayer University of Osijek.

    Google Scholar 

  • Luthria, D. L., Mukhopadhyay, S., & Krizek, D. T. (2006). Content of total phenolics and phenolic acids in tomato (Lycopersicon esculentum Mill.) fruits as influenced by cultivar and solar UV radiation. Journal of Food Composition and Analysis, 19(8), 771–777. https://doi.org/10.1016/j.jfca.2006.04.005.

    Article  CAS  Google Scholar 

  • Mahar, A., Wang, P., Ali, A., Awasthi, M. K., Lahori, A. H., Wang, Q., Li, R., & Zhang, Z. (2016). Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: a review. Ecotoxicology and Environmental Safety, 126, 111–121. https://doi.org/10.1016/j.ecoenv.2015.12.023.

    Article  CAS  Google Scholar 

  • Malekia, M., Ghorbanpourb, M., & Kariman, K. (2017). Physiological and antioxidative responses of medicinal plants exposed to heavy metals stress. Plant Gene, 11, 247–254. https://doi.org/10.1016/j.plgene.2017.04.006.

    Article  CAS  Google Scholar 

  • Michalak, A. (2006). Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish Journal of Environmental Studies, 15(4), 523–530.

    CAS  Google Scholar 

  • Ministry of Housing, Spatial Planning and Environment. (1994). The Netherlands’ national environmental policy Plan 2, VROM 93561/d//4-94 1221/027, The Hague, The Netherlands.

  • Mukhopadhyay, M. J., & Sharma, A. (1991). Manganese in cell metabolism of higher plants. The Botanical Review, 57(2), 117–149. https://doi.org/10.1007/BF02858767.

    Article  Google Scholar 

  • Nadgorska-Socha, A., Ptasinski, B., & Kita, A. (2012). Heavy metal bioaccumulation and antioxidative responses in Cardaminopsis arenosa and Plantago lanceolata leaves from metalliferous and non-metalliferous sites: a field study. Ecotoxicology, 22, 1422–1434. https://doi.org/10.1007/s10646-013-1129-y.

    Article  CAS  Google Scholar 

  • Nikolić, N., Kojić, D., Pilipović, A., Pajević, S., Krstić, B., Borišev, M., & Orlović, S. (2008). Responses of hybrid poplar to cadmium stress: photosynthetic characteristics, cadmium and proline accumulation, and antioxidant enzyme activity. Acta Biologica Cracoviensia Series Botanica, 50(2), 95–103.

    Google Scholar 

  • O’Dell, R. E., James, J. J., & Richards, H. (2006). Congeneric serpentine and nonserpentine shrubs differ more in leaf Ca:Mg than in tolerance of low N, low P, or heavy metals. Plant and Soil, 280, 49–64. https://doi.org/10.1007/s11104-005-3502-y.

    Article  CAS  Google Scholar 

  • Perez-Espinosa, A., Moreno-Caselles, J., Moral, R., Perez-Murcia, M. D., & Gomez, I. (2006). Effect of cobalt on chlorophyll and carotenoid contents in tomato plants. Journal of Plant Nutrition, 25(9), 1933–1940. https://doi.org/10.1081/PLN-120013285.

    Article  Google Scholar 

  • Rumball, W., Keogh, R. G., Lane, G. E., Miller, J. E., & Claydon, R. B. (1997). ‘Grasslands Lancelot’ plantain (Plantago lanceolata L.). New Zealand Journal of Agricultural Research, 40(3), 373–377. https://doi.org/10.1080/00288233.1997.9513258.

    Article  Google Scholar 

  • Samantaray, S., Rout, G. R., & Das, P. (2001). Induction, selection and characterization of Cr and Ni-tolerant cell lines of Echinochloa colona (L) in vitro. Journal of Plant Physiology, 158, 1281–1290. https://doi.org/10.1078/0176-1617-00533.

    Article  CAS  Google Scholar 

  • Shah, F. U. R., Ahmad, N., Masood, K. R., & Peralta-Videa, J. R. (2010). Heavy metal toxicity in plants. In M. Ashraf, M. Ozturk, & M. S. A. Ahmad (Eds.), Plant adaptation and phytoremediation. Dordrecht: Springer.

    Google Scholar 

  • Shakya, K., Chettri, M. K., & Sawidis, T. (2008). Impact of heavy metals (copper, zinc, and lead) on the chlorophyll content of some mosses. Archives of Environmental Contamination and Toxicology, 54, 412–421. https://doi.org/10.1007/s00244-007-9060-y.

    Article  CAS  Google Scholar 

  • Sharma, S. S., & Dietz, K. J. (2006). The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany, 57, 711–726. https://doi.org/10.1093/jxb/erj073.

    Article  CAS  Google Scholar 

  • Singh, O. V., Labana, S., Pandey, G., Budhiraja, R., & Jain, R. K. (2003). Phytoremediation: an overview of metallic ion decontamination from soil. Applied Microbiology and Biotechnology, 61, 405–412. https://doi.org/10.1007/s00253-003-1244-4.

    Article  CAS  Google Scholar 

  • Stanković, M. S. (2011). Total phenolic content, flavonoid concentration and antioxidant activity of Marrubium peregrinum L. extracts. Kragujevac Journal of Science, 33, 63–72.

    Google Scholar 

  • Stewart, A. V. (1996). Plantain (Plantago lanceolata) – a potential pasture species. Proceedings of the New Zealand Grassland Association, 58, 77–86.

    Google Scholar 

  • Suckling, D. M., Burnip, G. M., Walker, J. T. S., Shaw, P. W., McLaren, G. F., Howard, C. R., Lo, P., White, V., & Fraser, J. (1998). Abundance of leafrollers and their parasitoids on selected host plants in New Zealand. New Zealand Journal of Crop and Horticultural, 26(3), 193–203. https://doi.org/10.1080/01140671.1998.9514055.

    Article  Google Scholar 

  • Sun, R. L., Zhou, Q. Z., Sun, F. H., & Jin, C. X. (2007). Antioxidative defense and proline/phytochelatin accumulationin a newly discovered Cd-hyperaccumulator, Solanum nigrum L. Environmental and Experimental Botany, 60, 468–476. https://doi.org/10.1016/j.envexpbot.2007.01.004.

    Article  CAS  Google Scholar 

  • Szaufer-Hajdrych, M., & Goślińska, O. (2004). The quantitative determination of phenolic acids and antimicrobial activity of Symphoricarpus albus (L.) Blake. Acta Poloniae Pharmaceutica, 61(1), 69–74.

    CAS  Google Scholar 

  • Tashakor, M., Yaacob, W. Z. W., & Mohamad, H. (2011). Speciation and availability of Cr, Ni and Co in serpentine soils of Ranau, Sabah. American Journal of Geosciences, 2(1), 4–9.

    Google Scholar 

  • Ullah, R., Hadi, F., Ahmad, S., Jan, A. U., & Rongliang, Q. (2019). Phytoremediation of lead and chromium contaminated soil improves with the endogenous phenolics and proline production in Parthenium, Cannabis, Euphorbia, and Rumex species. Water Air and Soil Pollution, 230, 40. https://doi.org/10.1007/s11270-019-4089-x.

    Article  CAS  Google Scholar 

  • Vangronsveld, J., Herzig, R., Weyens, N., Boulet, J., Adriaensen, K., Ruttens, A., Thewys, T., Vassilev, A., Meers, E., Nehnevajova, E., Van der Lelie, D., & Mench, M. (2009). Phytoremediation of contaminated soils and groundwater: lessons from the field. Environmental Science and Pollution Research International, 16(7), 765–794. https://doi.org/10.1007/s11356-009-0213-6.

    Article  CAS  Google Scholar 

  • Verbruggen, N., Hermans, C., & Schat, H. (2009). Molecular mechanisms of metal hyperaccumulation in plants. New Phytologist, 181(4), 759–776. https://doi.org/10.1111/j.1469-8137.2008.02748.x.

    Article  CAS  Google Scholar 

  • Viehweger, K. (2014). How plants cope with heavy metals. Botanical Studies, 55, 35. https://doi.org/10.1186/1999-3110-55-35.

    Article  CAS  Google Scholar 

  • Weber, E. (2003). Invasive plant species of the world: a reference guide to environmental weeds. Wallingford: CAB International.

    Google Scholar 

  • Wu, W., Wu, P., Yang, F., Sun, D. L., Zhang, D. X., & Zhou, Y. K. (2018). Assessment of heavy metal pollution and human health risks in urban soils around an electronics manufacturing facility. Science of the Total Environment, 630, 53–61. https://doi.org/10.1016/j.scitotenv.2018.02.183.

    Article  CAS  Google Scholar 

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Ahatović, A., Čakar, J., Subašić, M. et al. Plantago lanceolata L. from Serpentine Soils in Central Bosnia Tolerates High Levels of Heavy Metals in Soil. Water Air Soil Pollut 231, 169 (2020). https://doi.org/10.1007/s11270-020-04561-7

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