Physiological Responses of Wetland Species Rumex Hydrolapathum to Increased Concentration of Biogenous Heavy Metals Zn and Mn in Substrate

Gederts Ievinsh 1 , Elīna Dišlere 1 , Andis Karlsons 2 , Anita Osvalde 2  and Māra Vikmane 1
  • 1 Faculty of Biology, University of Latvia, 1004, Rīga, Latvia
  • 2 Institute of Biology, University of Latvia, 2169, Salaspils, Latvia


The aim of the present study was to determine if individuals of Rumex hydrolapathum Huds native to saline wetlands are able to tolerate high concentration of biogenous heavy metals Zn and Mn in substrate and to accumulate high concentration of these metals in aboveground parts. Plant physiological status was monitored by using non-destructive analysis of chlorophyll and chlorophyll a fluorescence. R. hydrolapathum plants accumulated up to 1840 mg·kg−1 Zn and 6400 mg·kg−1 Mn in older leaves. The usefulness of monitoring changes in chlorophyll concentration and chlorophyll a fluorescence parameters to predict physiological response of R. hydrolapathum plants to excess Zn and Mn was not supported, as the lack of significant changes indicated that the model species showed adaptation to increased amount of metals in actively photosynthesizing tissues. It appears that Zn and Mn tolerance of R. hydrolapathum is based primarily at the physiological level where metal accumulation in younger leaves and roots is restricted, and development of new leaves is promoted together with induction of senescence in older leaves that have accumulated the majority of Zn and Mn. R. hydrolapathum can be characterised as a very promising model species for further studies for practical phytoremediation needs.

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  • Albert, R. (1975). Salt regulation in halophytes. Oecologia, 21, 57–71.

  • Anjum, N. A., Duarte, B., Caēador, I., Sleimi, N., Duarte, A. C., Pereira, E. (2016). Biophysical and biochemical markers of metal/metalloid impacts in salt marsh halophytes and their implications. Front. Environ. Sci., 4, 24.

  • Anjum, N. A., Singh, H. P., Khan, M. I. R., Masood, A., Per, T. S., Negi, A., Batish, D. R., Khan, N. A., Duarte, A. C., Pereira, E., Ahmad, I. (2015). Too much is bad — an appraisal of phytotoxicity of elevated plant beneficial heavy metal ions. Environ. Sci. Pollut. Res., 22, 3361–3382.

  • Baker, A. J. M., Brooks, R. R. (1989). Terrestrial higher plants which hyperaccumulate metallic elements — a review of their distribution, ecology and phytochemistry. Biorecovery, 1, 81–126.

  • Baker, N. R. (2006). A possible role for photosystem II in environmental perturbations of photosynthesis. Physiol. Plant., 81, 563–570.

  • Blaylock, M. J., Huang, J. W. (2000). Phytoextraction of metals. In: Raskin, I., Ensley, B. D. (eds.). Phytoremediation of Toxic Metals — Using Plants to Clean-up the Environment. Wiley, New York, pp. 53–70.

  • Bonanno, G., Vymazal, J., Cirelli, G. L. (2018). Translocation, accumulation and bioindication of trace elements in wetland plants. Sci. Total Environ., 631/632, 252–261.

  • Bothe, H., Sùomka, A. (2017). Divergent biology of facultative heavy metal plants. J. Plant Physiol., 219, 45–61.

  • Boyd, R. S. (2004). Ecology of metal hyperaccumulation. New Phytol., 162, 563–567.

  • Broadhurst, C. L., Chaney, R. L., Davis, A. P., Cox, A., Kumar, K,, Reeves, R. D., Green, C. E. (2015). Growth and cadmium phytoextraction by Swiss chard, maize, rice, Noccaea caerulescens, and Alyssum murale in pH adjusted biosolids amended soils. Int. J. Phytoremed., 17, 25–39.

  • Broadley, M. R., White, P. J., Hammond, J. P., Zelko, I., Lux, A. (2007). Zinc in plants. New Phytol., 173, 677–702.

  • Buscaroli, A. (2017). An overview of indexes to evaluate terrestrial plants for phytoremediation purposes (Review). Ecol. Indic., 82, 367–380.

  • Capra, G. F., Coppola, E., Odierna, P., Grilli, E., Vacca, S., Buondonno, A. (2014). Occurrence and distribution of key potentially toxic elements (PTEs) in agricultural soils: A paradigmatic case study in an area affected by illegal landfills. J. Geochem. Explor., 14, 169–180.

  • Clairmont, K. B., Hagar, W. G., Davis, E. A. (1986). Manganese toxicity to chlorophyll synthesis in tobacco callus. Plant. Physiol., 80, 291–293

  • Elamin, O. M., Wilcox, G. E. (1986). Effect of magnesium and manganese nutrition on muskmelon growth and manganese toxicity. J. Amer. Soc. Hortic. Sci., 111, 582–587.

  • Gao, W., Du, Y., Gao, S., Ingels, J., Wang, D. (2016). Heavy metal accumulation reflecting natural sedimentary processes and anthropogenic activities in two contrasting coastal wetland ecosystems, eastern China. J. Soils Sedim., 16, 1093–1108.

  • Guala, S. D., Vega, F. A., Covelo, E. F. (2011). Development of a model to select plants with optimum metal phytoextraction potential. Environ. Sci. Pollut. Res., 18, 997–1003.

  • Gupta, N., Ram, H., Kumar, G. (2016). Mechanism of Zn absorbtion in plants: Uptake, transport, translocation and accumulation. Rev. Environ. Sci. Biotechnol., 15, 89–109.

  • Hacisalihoglu, G., Kochian, L. V. (2003). How do some plants tolerate low levels of soil Zn? Mechanisms of zinc efficency in crop plants. New Phytol., 159, 341–350.

  • Hamed, K. B., Ellouzi, H., Talbi, O. Z., Hessini, K., Slama, I., Ghnaya, T., Bosch, S. M., Savoure, A., Abdelly, C. (2013). Physiological response of halophytes to multiple stresses. Funct. Plant Biol., 40, 883–896.

  • Han, R., Quinet, M., André, E., van Elteren, J. T., Destrebecq, F., Vogel-Mikuš, K., Cui, G., Debeljak, M., Lefčvre, I., Lutts, S. (2013). Accumulation and distribution of Zn in the shoots and reproductive structures of the halophyte plant species Kosteletzkya virginica as a function of salinity. Planta 238, 441–457.

  • Jain, R., Srivastava, S., Solomon, S., Shrivastava, A. K., Chandra, A. (2010). Impact of excess zinc on growth parameters, cell division, nutrient accumulation, photosynthetic pigments and oxidative stress of sugarcane (Saccharum spp.). Acta Physiol. Plant., 32, 979–986.

  • Javed, M. T., Stoltz, E., Lindberg, S., Greger, M. (2013). Changes in pH and organic acids in mucilage of Eriophorum angustifolium roots after exposure to elevated concentrations of toxic elements. Environ. Sci. Pollut. Res., 20, 1876–1880.

  • Jin, X. F., Yang, X. E., Islam, E., Liu, D., Mahmood, Q., Li, H., Li, J. (2008). Ultrastructural changes, zinc hyperaccumulation and its relation with anti-oxidants in two ecotypes of Sedum alfredii Hance. Plant Physiol. Biochem. 46, 997–1006.

  • Kalaji, H. M., Račková, L., Paganová, V., Swoczyna, T., Rusinowski, S., Sitko, K. (2018). Can chlorophyll-a fluorescence parameters be used as bio-indicators to distinguish between drought and salinity stress in Tilia cordata Mill? Environ. Exp. Bot., 152, 149–157.

  • Kan, X., Ren, J., Chen, T., Cui, M., Li, C., Zhou, R., Zhang, Y., Liu, H., Dexiang, D., Yin, Z. (2017). Effects of salinity on photosynthesis in maize probed by prompt fluorescence, delayed fluorescence and P700 signals. Environ. Exp. Bot., 140, 56–64.

  • Küpper, H., Zhao, F. J., McGrath, S. P. (1999). Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol., 119, 305–311.

  • Li, Q., Chen, L.-S., Jiang, H.-X., Tang, N., Yang, L.-T., Lin, Z.-H., Li, Y., Yang, G.-H. (2010). Effects of manganese-excess on CO2 assimilation, ribulose-1,5-bisphosphate carboxylase/oxygenase, carbohydrates and photosynthetic electron transport of leaves, and antioxidant systems of leaves and roots in Citrus grandis seedlings. BMC Plant Biol., 10, 42.

  • Li, T.-Q., Yang, Z. E., Yang, J.-Y., He, Z.-L. (2006). Zn accumulation and subcellular distribution in the Zn hyperaccumulator Sedum alfredii Hance. Pedosphere, 16, 616–623.

  • Liang, H. M., Lin, T. H., Chiou, J. M., Yeh, K. C. (2009). Model evaluation of the phytoextraction potential of heavy metal hyperaccumulators and non-hyperaccumulators. Environ. Pollut., 157, 1945–1952.

  • Liang, L., Liu, W., Sun, Y., Huo, X., Li, S., Zhou, Q. (2017). Phytoremediation of heavy metal contaminated saline soils using halophytes: Current progress and future perspectives. Environ. Res., 25, 269–281.

  • Liu, J., Shang, W., Zhang, Zhu, Y., Yu, K. (2014). Mn accumulation and tolerance in Celosia argentea Linn.: A new Mn-hyperaccumulating plant species. J. Hazard. Mater., 267, 136–141.

  • Liu, P., Tang, X., Gong, C., Xu, G. D. (2010). Manganese tolerance and accumulation in six Mn hyperaccumulators or accumulators. Plant Soil, 335, 285–395.

  • Loneragan, J. F. (1988). Distribution and movement of manganese in plants. In: Graham, R. D., Hannam, R. J., Uren, N. C. (eds.). Manganese in Soils and Plants. Developments in Plant and Soil Sciences, Vol 33. Springer, Dordrecht, pp. 113–124.

  • Longnecker, N. E., Robson, A. D. (1993). Distribution and transport of zinc in plants. In: Robson, A. D. (ed.). Zinc in Soils and Plants. Developments in Plant and Soil Sciences, Vol 55. Springer, Dordrecht, pp. 79–91.

  • Lutts, S., Levčvre, I. (2015). How can we take advantage of halophyte properties to cope with heavy metal toxicity in salt-affected areas. Ann. Bot., 115, 509–528.

  • Masarovičová, E., Králová, K., Kummerová, M. (2010). Principles of classification of medicinal plants as hyperaccumulators or excluders. Acta Physiol. Plant., 32, 823–829.

  • Mateos-Naranjo, E., Redondo-Gómez, S., Cambrollé, J., Luque, T., Fugeroa, M. E. (2008). Growth and photosynthetic responses to zinc stress of an invasive cordgrass Spartina densiflora. Plant Biol., 10, 754–762.

  • Mitchell, R. G., Spliethoff, H. M., Ribaudo, L. N., Lopp, D. M., Shayler, H. A., Marquez-Bravo, L. G., Lambert, V. T., Ferenz, G. S., Russell-Anelli, J. M., Stone, E. B., McBride, M. B. (2014). Lead (Pb) and other metals in New York City community garden soils: Factors influencing contaminant distributions. Environ. Pollut., 187, 162–169.

  • Moray, C., Goolsbay, E. W., Bromham, L. (2016). The phylogenetic association between salt tolerance and heavy metal hyperaccumulation in Angiosperms. Evol. Biol., 43, 119–130.

  • Naidu, R., Oliver, D., McConnell, S. (2003). Heavy metal phytotoxicity in soils. In: Proceedings of the Fifth National Workshop on the Assessment of Site Contamination. Environment Protection & Heritage Council, Adelaide, pp. 235–241.

  • Osvalde, A. (2011). Optimization of plant mineral nutrition revisited: The roles of plant requirements, nutrient interactions, and soil properties in fertilization management. Environ. Exp. Biol., 9, 1–8.

  • Peng, D., Shafi, M., Wang, Y., Li, S., Yan, W., Chen, J., Ye, Z., Liu, D. (2015). Effect of Zn stresses on physiology, growth, Zn accumulation, and chlorophyll of Phyllostachys pubescens. Environ. Sci. Pollut. Res., 22, 14983–14992.

  • Pinto, E., Aguiar, A. R. M., Ferreura I. M. P. L. V. O. (2014). Influence of soil chemistry and plant physiology in the phytoremediation of Cu, Man, and Zn. Crit. Rev. Plant Sci., 33, 351–373.

  • Rascio, N., Navari-Izzo, F. (2011). Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? Plant Sci., 180, 169–181.

  • Reeves, R. D., van der Ent, A., Baker, A. J. M. (2018). Global distribution and ecology of hyperaccumulator plants. In: van der Ent, A., Echevarria, G., Baker, A., Morel, J. (eds.). Agromining: Farming for Metals. Mineral Resource Reviews. Springer International Publishing, Cham, pp. 75–92.

  • Reeves, R. D., Baker, A. J. M., Jaffré, T., Erskine, P. D., Echevarria, G., van der Ent, A. (2017). A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol., 218, 407–411.

  • Reichman, S. (2002). The Responses of Plant to Metal Ttoxicity: A Review Focusing on Copper, Manganese and Zinc. Australian Minerals & Energy Environment Foundation, Melbourne. 54 pp.

  • Ren, F., Liu, T., Liu, H., Hu, B. (1993). Influence of zinc on the growth, distribution of elements, and metabolism of one-year old American ginseng plants. J. Plant Nutr., 16, 393–405.

  • Samsone, I., Ievinsh, G. (2018). Different plant species accumulate various concentration of Na+ in a sea-affected coastal wetland during a vegetation season. Environ. Exp. Biol., 16, 117–127.

  • Santos, E. F., Santini, J. M. K., Paixćo, A. P., Jśnior, E. F., Lavres, J., Campos, M., dos Reis, A. R. (2017). Physiological highlights of manganese toxicity symptoms in soybean plants: Mn toxicity responses. Plant Physiol. Biochem., 113, 6–19.

  • Sghaier, D. B., Duarte, B., Bankaji, I., Caēador, I., Sleimi, N. (2015). Growth, chlorophyll fluorescence and mineral nutrition in the halophyte Tamarix gallica cultivated in combined stress conditions: Arsenic and NaCl. J. Photochem. Photobiol. B Biol., 149, 204–214.

  • Shen, Z. G., Zhao, F. J., McGrath, S. P. (1997). Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non-hyper-accumulator Thlaspi ochroleucum. Plant Cell Environ., 20, 898–906.

  • Sruthi, P., Shackira, A. M., Puthur, J. T. (2017). Heavy metal detoxification mechanisms in halophytes: An overview. Wetlands Ecol. Manag., 25, 129–148.

  • Strasser, R. J., Srivastava, A., Tsimilli-Michael, M. (2000). The fluorescence transient as a tool to characterise and screen photosynthetic samples. In: Yunus, M., Pathre, U., Mohanty, P. (eds.). Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Taylor & Francis, London, pp. 445–483

  • Tang, S., Fang, Y. (2012). Copper accumulation by Polygonum micro-cephalum D. Don and Rumex hastatus D. Don from copper mine spoils in Yunnan Province, P. R. China. Environ. Geol., 40, 902–907.

  • Tang, Y.-T., Qiu, R.-L., Zeng, X-.W., Ying, R.-R., Yu, F.-M., Zhou, X.-Y. (2009). Lead, zinc, cadmium hyperaccumulation and growth stimulation in Arabis paniculata Franch. Environ. Exp. Bot., 66, 126–134.

  • Van Oosten, M. J., Maggio, A. (2015). Functional biology of halophytes in the phytoremediation of heavy metal contaminated soils. Environ. Exp. Bot., 111, 135–146.

  • Visioli, G., Marmiroli, N. (2013). The proteomics of heavy metal hyperaccumulation in plants. J. Proteom., 79, 133–145.

  • Vondráčková, S., Hejcman, M., Száková, J., Müllerová, V., Tlustoš, P. (2014). Soil chemical properties affect the concentration of elements (N, P, K, Ca, Mg, As, Cd, Cr, Cu, Fe, Mn, Ni, Pb, and Zn) and their distribution between organs of Rumex obtusifolius. Plant Soil, 379, 231–245.

  • Vondráčková, S., Száková, J., Drábek, O., Tejnecký, V., Hejcman, M., Müllerová, V., Tlustoš, P. (2015). Aluminium uptake and translocation in Al hyperaccumulator Rumex obtusifolius is affected by low-molecular weight organic acids content and soil pH. PLOS One, 10, e0123351.

  • Wang, A. S., Angle, J. S., Rufus, L. C., Delorme, T. A., Reeves, R. D. (2006). Soil pH effects on uptake of Cd and Zn by Thlaspi caerulencens. Plant Soil, 281, 325–337.

  • Wang, C., Zhang, S. H., Wang, P. F., Hou, J., Zhang, W. J., Li, W., Lin, Z. P. (2009). The effect of excess Zn on mineral nutrition and antioxidative response in rapeseed seedlings. Chemosphere, 75, 1468–1476.

  • Xue, S. G., Chen, Y. X., Reeves, R. D., Baker, A. J. M., Lin, Q., Fernando, D. R. (2004). Manganese uptake and accumulation by the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Environ. Pollut., 131, 393–399.

  • Yang, J., Ye, Z. (2009). Metal accumulation and tolerance in wetland plants. Front. Biol. China, 4, 282–288.

  • Yang, W., Li, H., Zhang, T., Sen, L., Ni, W. (2014). Classification and identification of metal-accumulating plant species by cluster analysis. Environ. Sci. Pollut. Res., 21, 10626–10637.

  • Ye, M., Liao, B., Li, J. T., Mengoni, A., Hu, M., Luo, W. C., Shu, W. S. (2012). Contrasting patterns of genetic divergence in two sympatric pseudo-metallophytes: Rumex acetosa L. and Commelina communis L. BMC Evol. Biol., 12, 84.

  • Zhuang, P., Wang, Q. W., Wang, H. B., Shu, W. S. (2007). Phytoextraction of heavy metals by eight plant species in field. Water Air Soil Pollut., 184, 235–242.


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