Abstract
Antimony (Sb) pollution has become a pressing environmental problem in recent years. Trees have been proven to have great potential for the feasible phytomanagement; however, little is known about Sb retention and tolerance in trees. The Chinese cork oak (Quercus variabilis Bl.) is known to be capable of growth in soils containing high concentrations of Sb. This study explored in detail the retention and acclimation of Q. variabilis under moderate and high external Sb levels. Results revealed that Q. variabilis could tolerate and accumulate high Sb (1623.39 mg kg−1 DW) in roots. Dynamics of Sb retention in leaves, stems, and roots of Q. variabilis were different. Leaf Sb remained at a certain level for several weeks, while in roots and stems, Sb concentrations continued to increase. Sb damaged tree’s PSII reaction cores but elicited defense mechanism at the donor side of PSII. It affected the electron transport flow after QA − more strongly than the oxygen-evolving complex and light-harvesting pigment-protein complex II. Sb also decreased leaf chlorophyll concentrations and therefore inhibited plant growth. During acclimation to Sb toxicity, Sb concentrations in leaves, stems, and roots decreased, with photosynthetic activity and pigments recovering to normal levels by the end of the experiment. These findings suggest that Sb tolerance in Q. variabilis is inducible. Acclimation seems to be related to homeostasis of Sb in plants. Results of this study can provide useful information for trees breeding and selection of Sb phytomanagement strategies, exploiting the established ability of Q. variabilis to transport, delocalize in the leaves, and tolerate Sb pollutions.
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References
An YJ, Kim M (2009) Effect of antimony on the microbial growth and the activities of soil enzymes. Chemosphere 74:654–659
Appenroth KJ, Stockel J, Srivastava A, Strasser RJ (2001) Multiple effects of chromate on the photosynthetic apparatus of Spirodela polyrhiza as probed by OJIP chlorophyll a fluorescence measurements. Environ Pollut 115:49–64
Arrivault S, Senger T, Kramer U (2006) The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J 46:861–879
Assunção AG, Pieper B, Vromans J, Lindhout P, Aarts MG, Schat H (2006) Construction of a genetic linkage map of Thlaspi caerulescens and quantitative trait loci analysis of zinc accumulation. New Phytol 170:21–32
Baker AJM (1981) Accumulators and excluders—strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654
Baker AJM (1987) Metal tolerance. New Phytol 106:93–111
Barberon M, Zelazny E, Robert S, Conéjéro G, Curie C, Friml J, Vert G (2011) Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc Natl Acad Sci 108(32):E450–E458
Barona A, Aranguiz I, Elias A (2001) Metal associations in soils before and after EDTA extractive decontamination: implications for the effectiveness of further clean-up procedures. Environ Pollut 113:79–85
Bazihizina N, Taiti C, Marti L, Rodrigo-Moreno A, Spinelli F, Giordano C, Caparrotta S, Gori M, Azzarello E, Mancuso S (2014) Zn2+-induced changes at the root level account for the increased tolerance of acclimated tobacco plants. J Exp Bot 65(17):4931–4942
Dickinson NM, Pulford ID (2005) Cadmium phytoextraction using short-rotation coppice Salix: the evidence trail. Environ Int 31:609–613
Domínguez MT, Maranón T, Murillo JM, Schulin R, Robinson BH (2008) Trace element accumulation in woody plants of the Guadiamar Valley, SW Spain: a large-scale phytomanagement case study. Environ Pollut 152(1):50–59
Domínguez MT, Madrid F, Marañón T, Murillo JM (2009) Cadmium availability in soil and retention in oak roots: potential for phytostabilization. Chemosphere 76:480–486
Evangelou MWH, Ebel M, Schaeffer A (2007) Chelate assisted phytoextraction of heavy metals from soil. Effect, mechanism, toxicity, and fate of chelating agents. Chemosphere 68:989–1003
Evangelou MWH, Robinson BH, Gunthardt-Goerg MS, Schulin R (2013) Metal uptake and allocation in trees grown on contaminated land: implications for biomass production. Int J Phytorem 15:77–90
Fasani E (2012) Plants that hyperaccumulate heavy metals. In: Furini A (ed) Plants and heavy metals. Springer, Netherlands, pp 55–74
Fässler E, Robinson BH, Stauffer W, Gupta SK, Papritz A, Schulin R (2010) Phytomanagement of metal-contaminated agricultural land using sunflower, maize and tobacco. Agric Ecosyst Environ 136(1):49–58
Feng R, Wei C, Tu S, Wu F, Yang L (2009) Antimony accumulation and antioxidative responses in four fern plants. Plant Soil 317:93–101
Feng R, Wei C, Tu S, Tang S, Wu F (2011) Detoxification of antimony by selenium and their interaction in paddy rice under hydroponic conditions. Microchem J 97:57–61
Fernández-Falcón M, Hernández M, Alvarez CE, Borges AA (2006) Variation in nutrition along time and relative chlorophyll content of Leucospermum cordifolium cv. ‘High Gold’, and their relationship with chlorotic sypmptoms. Sci Hortic-Amsterdam 107:373–379
Filella M, Belzile N, Chen Y (2002) Antimony in the environment: a review focused on natural waters: I. Occurrence. Earth-Sci Rev 57:125–176
Furnholm TR, Tisa LS (2014) The ins and outs of metal homeostasis by the root nodule actinobacterium Frankia. BMC Genomics 15(1):1092
Gebel T, Christensen S, Dunkelberg H (1997) Comparative and environmental genotoxicity of antimony and arsenic. Anticancer Res 17:2603–2607
Gogorcena Y, Larbi A, Andaluz S, Carpena RO, Abadia A, Abadia J (2011) Effects of cadmium on cork oak (Quercus suber L.) plants grown in hydroponics. Tree Physiol 31:1401–1412
Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta Biomembr 1465(1–2):190–198
He M, Yang J (1999) Effects of different forms of antimony on rice during the period of germination and growth and antimony concentration in rice tissue. Sci Total Environ 243–244:149–155
He J, Ma C, Ma Y, Li H, Kang J, Liu T (2012a) Cadmium tolerance in six poplar species. Environ Sci Pollut Res 20(1):163–174
He M, Wang X, Wu F, Fu Z (2012b) Antimony pollution in China. Sci Total Environ 421–422:41–50
Janik E, Maksymiec W, Mazur R, Garstka M, Gruszecki WI (2010) Structural and functional modifications of the major light-harvesting complex II in cadmium- or copper-treated Secale cereale. Plant Cell Physiol 51:1330–1340
Kawachi M, Kobae Y, Mori H, Tomioka R, Lee Y, Maeshima M (2009) A mutant strain Arabidopsis thalianathat lacks vacuolar membrane zinc transporter MTP1 revealed the latent tolerance to excessive zinc. Plant Cell Physiol 50:1156–1170
Kerkeb L, Mukherjee I, Chatterjee I, Lahner B, Salt DE, Connolly EL (2008) Iron-induced turnover of the Arabidopsis IRON-REGULATED TRANSPORTER1 metal transporter requires lysine residues. Plant Physiol 146(4):1964–1973
Kobae Y, Uemura T, Sato M, Ohnishi M, Mimura T, Nakagawa T, Maeshima M (2004) Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol 45:1749–1758
Krachler M, Emons H, Zheng J (2001) Speciation of antimony for the 21st century: promises and pit falls. TrAC Trends Anal Chem 20:79–90
Krachler M, Zheng J, Koerner R, Zdanowicz C, Fisher D, Shotyk W (2005) Increasing atmospheric antimony contamination in the northern hemisphere: snow and ice evidence from Devon Island, Arctic Canada. J Environ Monit 7:1169–1176
Krämer U, Talke I, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272
Lin YF, Aarts MG (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69(19):3187–3206
Maher WA (2009) Antimony in the environment-the new global puzzle. Environ Chem 6:93–94
Mills RF, Krijger GC, Baccarini PJ, Hall J, Williams LE (2003) Functional expression of AtHMA4, a P1B-type ATPase of the Zn/Co/Cd/Pb subclass. Plant J 35(2):164–176
Oukarroum A, Madidi SE, Schansker G, Strasser RJ (2007) Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. Environ Exp Bot 60:438–446
Pan X, Zhang D, Chen X, Bao A, Li L (2011) Antimony accumulation, growth performance, antioxidant defense system and photosynthesis of Zea mays in response to antimony pollution in soil. Water Air Soil Pollut 215:517–523
Paoli L, Fiorini E, Munzi S, Sorbo S, Basile A, Loppi S (2013) Antimony toxicity in the lichen Xanthoria parietina (L.) Th. Fr. Chemosphere 93:2269–2275
Parraga-Aguado I, Gonzalez-Alcaraz MN, Alvarez-Rogel J, Jimenez-Carceles FJ, Conesa HM (2013) The importance of edaphic niches and pioneer plant species succession for the phytomanagement of mine tailings. Environ Pollut 176:134–143
Pinto ISS, Neto IFF, Soares HMVM (2014) Biodegradable chelating agents for industrial, domestic, and agricultural applications—a review. Environ Sci Pollut Res 21(20):11893–11906
Prasad MN, Freitas H (2000) Removal of toxic metals from solution by leaf, stem and root phytomass of Quercus ilex L. (holly oak). Environ Pollut 110:277–283
Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees—a review. Environ Int 29:529–540
Puschenreiter M, Turktas M, Sommer P, Wieshammer G, Laaha G, Wenzel WW, Hauser MT (2010) Differentiation of metallicolous and non-metallicolous Salix caprea populations based on phenotypic characteristics and nuclear microsatellite (SSR) markers. Plant Cell Environ 33:1641–1655
Robinson BH, Bañuelos G, Conesa HM, Evangelou MW, Schulin R (2009) The phytomanagement of trace elements in soil. Crit Rev Plant Sci 28(4):240–266
Shtangeeva I, Steinnes E, Lierhagen S (2012) Uptake of different forms of antimony by wheat and rye seedlings. Environ Sci Pollut Res 19(2):502–509
Smichowski P (2008) Antimony in the environment as a global pollutant: a review on analytical methodologies for its determination in atmospheric aerosols. Talanta 75:2–14
Steely S, Amarasiriwardena D, Xing B (2007) An investigation of inorganic antimony species and antimony associated with soil humic acid molar mass fractions in contaminated soils. Environ Pollut 148:590–598
Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B 104:236–257
Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42
Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou G, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Netherlands, pp 321–362
Sun F, Yan Y, Liao H, Bai Y, Xing B, Wu F (2014) Biosorption of antimony (V) by freshwater cyanobacteria Microcystis from Lake Taihu, China: effects of pH and competitive ions. Environ Sci Pollut Res 21(9):5836–5848
Toth SZ, Schansker G, Garab G, Strasser RJ (2007) Photosynthetic electron transport activity in heat-treated barley leaves: the role of internal alternative electron donors to photosystem II. Biochim Biophys Acta 1767:295–305
Toth SZ, Puthur JT, Nagy V, Garab G (2009) Experimental evidence for ascorbate-dependent electron transport in leaves with inactive oxygen-evolving complexes. Plant Physiol 149:1568–1578
Tschan M, Robinson BH, Nodari M, Schulin R (2009a) Antimony uptake by different plant species from nutrient solution, agar and soil. Environ Chem 6:144–152
Tschan M, Robinson BH, Schulin R (2009b) Antimony in the soil-plant system-a review. Environ Chem 6:106–115
Tschan M, Robinson B, Johnson CA, Bürgi A, Schulin R (2010) Antimony uptake and toxicity in sunflower and maize growing in SbIII and SbV contaminated soil. Plant Soil 334:235–245
United States Environmental Protection Agency (1979) Toxics release inventory. Doc. 745-R-00-007. USEPA, Washington, DC, USA
Wasay SA, Barrington SF, Tokunaga S (1998) Remediation of soils polluted by heavy metals using salts of organic acids and chelating agents. Environ Technol 19:369–379
Williams LE, Mills RF (2005) P1B-ATPases—an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10(10):491–502
Xue L, Liu J, Shi S, Wei Y, Chang E, Gao M, Chen L, Jiang Z (2014) Uptake of heavy metals by native herbaceous plants in an antimony mine (Hunan, China). Clean: Soil, Air, Water 42(1):81–87
Yusuf MA, Kumar D, Rajwanshi R, Strasser RJ, Tsimilli-Michael M, Govindjee Sarin NB (2010) Overexpression of gamma-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. Biochim Biophys Acta 1797:1428–1438
Zhao X, Liu J, Xia X, Chu J, Wei Y, Shi S, Chang E, Yin W, Jiang Z (2014) The evaluation of heavy metal accumulation and application of a comprehensive bio-concentration index for woody species on contaminated sites in Hunan, China. Environ Sci Pollut Res 21:5076–5085
Zurek G, Rybk K, Pogrzeba M, Krzyzak J, Prokopiuk K (2014) Chlorophyll a fluorescence in evaluation of the effect of heavy metal soil contamination on perennial grasses. PLoS One 9:e91475
Acknowledgments
The authors are grateful to Dr. Fang-Ping Tong and Zhen-Hua Liu at the Research Institute of Forestry, Hunan Academy of Forestry, China, for their continuous support during the experiment, and to the anonymous referee for his helpful comments on this manuscript.
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This work was supported by the Project from Ministry of Science and Technology, China (2012BAC09B03 and 2011BAD38B0103) and Beijing Natural Science Foundation (No.8152032).
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The authors declare that they have no conflict of interest.
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Zhao, X., Zheng, L., Xia, X. et al. Responses and acclimation of Chinese cork oak (Quercus variabilis Bl.) to metal stress: the inducible antimony tolerance in oak trees. Environ Sci Pollut Res 22, 11456–11466 (2015). https://doi.org/10.1007/s11356-015-4304-2
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DOI: https://doi.org/10.1007/s11356-015-4304-2