Environ Sci Pollut Res DOI 10.1007/s11356-015-4304-2
RESEARCH ARTICLE
Responses and acclimation of Chinese cork oak (Quercus variabilis Bl.) to metal stress: the inducible antimony tolerance in oak trees Xiulian Zhao & Lingyu Zheng & Xinli Xia & Weilun Yin & Jingpin Lei & Shengqing Shi & Xiang Shi & Huiqing Li & Qinghe Li & Yuan Wei & Ermei Chang & Zeping Jiang & Jianfeng Liu
Received: 4 November 2014 / Accepted: 2 March 2015 # Springer-Verlag Berlin Heidelberg 2015
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 pig-
ment-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.
Responsible editor: Philippe Garrigues
Introduction
X. Zhao : L. Zheng : J. Lei : S. Shi : X. Shi : H. Li : Q. Li : Y. Wei : E. Chang : Z. Jiang : J. Liu (*) State Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, People’s Republic of China e-mail: [email protected] X. Zhao : L. Zheng : S. Shi Key Laboratory of Tree Breeding and Cultivation, State Forestry Administration, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, People’s Republic of China X. Zhao : X. Xia : W. Yin (*) College of Biology, National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, People’s Republic of China e-mail: [email protected]
Keywords Heavy metal pollution . Phytoremediation . Tolerance . Chlorophyll fluorescence . Acclimation
Heavy metal pollution is ubiquitous in industrialized environments and has become one of the most serious environmental problems currently facing mankind. Antimony (Sb) is a major heavy metal pollutant, which has been increasing in the environment at an alarming rate in recent years (Krachler et al. 2001; Tschan et al. 2009b). For example, Sb concentrations in arctic snow and ice have increased by 50 % over the past 30 years (Krachler et al. 2005). Since the Industrial Revolution, the use of Sb has drastically increased as a result of its application in car brake linings and fire retardants (Maher 2009) and as a hardening agent in bullet alloys (2– 5 % Sb) (Steely et al. 2007). An increase in Sb mining and smelting processes has also resulted in the release of large
Environ Sci Pollut Res
quantities of Sb, resulting in serious Sb contamination of local environments (He et al. 2012a, b). Sb has no known biological function and displays hazardous to human health or even carcinogenic properties (Gebel et al. 1997). Its inorganic form is more toxic than the organic form, with SbIII being 10 times more toxic than SbV (Smichowski 2008). Due to its high potential environmental toxicity, Sb compounds have been listed as pollutants of priority interest by the United States Environmental Protection Agency (USEPA 1979) and were labeled as hazardous waste by the European Union (EU) Basel convention (Filella et al. 2002). In recent years, Sb has been recognized as a global pollutant and has become a hot topic in the international science community (e.g., Steely et al. 2007; Shtangeeva et al. 2012; Sun et al. 2014). Phytomanagement is the use of vegetation and soil amendments to reduce the environmental risk posed by contaminated sites. It includes all biological, chemical, and physical technologies employed on a vegetated site. Successful phytomanagement should either cost less than other remediation or fortification technologies, or be a profitable operation, by producing valuable plant biomass products (Robinson et al. 2009). Because of its elegance and the vast extent of contaminated areas to which it may be applied, it has received significant scientific and commercial attention (e.g., Domínguez et al. 2008; Fässler et al. 2010; Parraga-Aguado et al. 2013). To revegetate the emergent Sb polluted sites, understanding the behavior of Sb in plants is important, particularly the mechanisms involved in Sb retention and tolerance in highly Sb-tolerant plants. In the last decade, related research has focused on Sb damage in plants, especially in crops. For example, Sb has been reported to inhibit growth (root growth and sprouts) of rice and wheat and reduce rice yield (He and Yang 1999). It may affect photosynthesis of maize, specifically by inhibiting chlorophyll synthesis and reducing maximum photochemical efficiency (Fv/Fm) (Pan et al. 2011). Elevated malondialdehyde concentrations, which enhanced the extent of lipid peroxidation, were also observed in rice and maize (Feng et al. 2011). Recently, researchers observed that the biomass of fern species also decreased significantly (P
RESEARCH ARTICLE
Responses and acclimation of Chinese cork oak (Quercus variabilis Bl.) to metal stress: the inducible antimony tolerance in oak trees Xiulian Zhao & Lingyu Zheng & Xinli Xia & Weilun Yin & Jingpin Lei & Shengqing Shi & Xiang Shi & Huiqing Li & Qinghe Li & Yuan Wei & Ermei Chang & Zeping Jiang & Jianfeng Liu
Received: 4 November 2014 / Accepted: 2 March 2015 # Springer-Verlag Berlin Heidelberg 2015
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 pig-
ment-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.
Responsible editor: Philippe Garrigues
Introduction
X. Zhao : L. Zheng : J. Lei : S. Shi : X. Shi : H. Li : Q. Li : Y. Wei : E. Chang : Z. Jiang : J. Liu (*) State Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, People’s Republic of China e-mail: [email protected] X. Zhao : L. Zheng : S. Shi Key Laboratory of Tree Breeding and Cultivation, State Forestry Administration, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, People’s Republic of China X. Zhao : X. Xia : W. Yin (*) College of Biology, National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, People’s Republic of China e-mail: [email protected]
Keywords Heavy metal pollution . Phytoremediation . Tolerance . Chlorophyll fluorescence . Acclimation
Heavy metal pollution is ubiquitous in industrialized environments and has become one of the most serious environmental problems currently facing mankind. Antimony (Sb) is a major heavy metal pollutant, which has been increasing in the environment at an alarming rate in recent years (Krachler et al. 2001; Tschan et al. 2009b). For example, Sb concentrations in arctic snow and ice have increased by 50 % over the past 30 years (Krachler et al. 2005). Since the Industrial Revolution, the use of Sb has drastically increased as a result of its application in car brake linings and fire retardants (Maher 2009) and as a hardening agent in bullet alloys (2– 5 % Sb) (Steely et al. 2007). An increase in Sb mining and smelting processes has also resulted in the release of large
Environ Sci Pollut Res
quantities of Sb, resulting in serious Sb contamination of local environments (He et al. 2012a, b). Sb has no known biological function and displays hazardous to human health or even carcinogenic properties (Gebel et al. 1997). Its inorganic form is more toxic than the organic form, with SbIII being 10 times more toxic than SbV (Smichowski 2008). Due to its high potential environmental toxicity, Sb compounds have been listed as pollutants of priority interest by the United States Environmental Protection Agency (USEPA 1979) and were labeled as hazardous waste by the European Union (EU) Basel convention (Filella et al. 2002). In recent years, Sb has been recognized as a global pollutant and has become a hot topic in the international science community (e.g., Steely et al. 2007; Shtangeeva et al. 2012; Sun et al. 2014). Phytomanagement is the use of vegetation and soil amendments to reduce the environmental risk posed by contaminated sites. It includes all biological, chemical, and physical technologies employed on a vegetated site. Successful phytomanagement should either cost less than other remediation or fortification technologies, or be a profitable operation, by producing valuable plant biomass products (Robinson et al. 2009). Because of its elegance and the vast extent of contaminated areas to which it may be applied, it has received significant scientific and commercial attention (e.g., Domínguez et al. 2008; Fässler et al. 2010; Parraga-Aguado et al. 2013). To revegetate the emergent Sb polluted sites, understanding the behavior of Sb in plants is important, particularly the mechanisms involved in Sb retention and tolerance in highly Sb-tolerant plants. In the last decade, related research has focused on Sb damage in plants, especially in crops. For example, Sb has been reported to inhibit growth (root growth and sprouts) of rice and wheat and reduce rice yield (He and Yang 1999). It may affect photosynthesis of maize, specifically by inhibiting chlorophyll synthesis and reducing maximum photochemical efficiency (Fv/Fm) (Pan et al. 2011). Elevated malondialdehyde concentrations, which enhanced the extent of lipid peroxidation, were also observed in rice and maize (Feng et al. 2011). Recently, researchers observed that the biomass of fern species also decreased significantly (P
