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This Article Appeared in a Journal Published by Elsevier. the Attached This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Journal of Plant Physiology 170 (2013) 355–359 Contents lists available at SciVerse ScienceDirect Journal of Plant Physiology j ournal homepage: www.elsevier.com/locate/jplph Short communication Non-invasive microelectrode cadmium flux measurements reveal the spatial characteristics and real-time kinetics of cadmium transport in hyperaccumulator and nonhyperaccumulator ecotypes of Sedum alfredii a b,c,∗ b,c b,c d Jian Sun , Ruigang Wang , Zhongqi Liu , Yongzhen Ding , Tingqiang Li a College of Life Science, Jiangsu Normal University, Xuzhou 221116, Jiangsu Province, PR China b Center for Research in Ecotoxicology and Environmental Remediation, Agro-environmental Protection Institute, Ministry of Agriculture, Tianjin 300191, PR China c Open Key Laboratory of Agro-environment and Food Safety of the Ministry of Agriculture, Tianjin 300191, PR China d Ministry of Education Key Laboratory of Environmental Remediation and Ecological Health, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, PR China a r t i c l e i n f o a b s t r a c t Article history: This study aims to determine the spatial characteristics and real-time kinetics of cadmium transport in Received 17 May 2012 hyperaccumulator (HE) and nonhyperaccumulator (NHE) ecotypes of Sedum alfredii using a non-invasive Received in revised form 16 October 2012 Cd-selective microelectrode. Compared with the NHE S. alfredii, the HE S. alfredii showed a higher Cd Accepted 17 October 2012 influx in the root apical region and root hair cells, as well as a significantly higher Cd efflux in the leaf petiole after root pre-treatment with cadmium chloride (CdCl2). Thus, HE S. alfredii has a higher capability Keywords: for the translocation of absorbed Cd to the shoot. Moreover, the mesophyll tissues, isolated mesophyll Sedum alfredii protoplasts, and intact vacuoles from HE S. alfredii exhibited an instantaneous influx of Cd in response to Cadmium flux CdCl2 treatment with mean rates that are markedly higher than those from NHE S. alfredii. Therefore, the Root hair cell hyper-accumulating trait of HE S. alfredii is characterized by the rapid Cd uptake in specific root regions, Intact vacuole Root-to-shoot translocation including the apical region and root hair cells, as well as by the rapid root-to-shoot translocation and the highly efficient Cd-permeable transport system in the plasma membrane and mesophyll cell tonoplast. We suggest that the non-invasive Cd-selective microelectrode is an excellent method with a high degree of spatial resolution for the study of Cd transport at the tissue, cellular, and sub-cellular levels in plants. © 2012 Elsevier GmbH. All rights reserved. Introduction Thlaspi praecox, and Sedum alfredii. Since then, significant progress has been made in understanding the physiological and molec- Cadmium (Cd), a non-essential heavy metal widely presents ular mechanisms of Cd hyperaccumulation (Verbruggen et al., in the environment, is a pollutant that is highly toxic to all 2009). living cells (Pilon-Smits, 2005; Mohanty et al., 2010). Previous The progress in this field depends on the development of related studies suggested that phytoremediation using hyper accumu- techniques to analyze Cd transport in plants. Of these methods, 109 lator plants that can grow in contaminated soils is a useful radiotracer Cd experiments, X-ray microfluorescence imaging, technique to reduce or remove soil Cd contamination. The hyper- and Cd-sensitive fluorescent probe imaging have been widely accumulator plants reduce the soil Cd content by translocation adopted and proven effective in the study of the flux and in vivo and accumulating high concentrations of the heavy metal in localization of Cd in plants (Lu et al., 2008; Lu, 2008; Tian et al., their shoots (Pilon-Smits, 2005; Mohanty et al., 2010). In the last 2011). Recent studies utilized the non-invasive measurement of ion decade, several plant species were identified as Cd hyperaccumu- fluxes to elucidate the dynamic changes in ion relations induced by lators, including Noccaea (Thlaspi) caerulescens, Arabidopsis halleri, environmental stresses. To date, two typical but similar techniques designed to measure ion fluxes across membranes have been devel- oped, namely, the scanning ion-selective electrode technique (SIET) and the microelectrode ion flux estimation (MIFE) technique. SIET Abbreviations: Cd, cadmium; HE, hyper accumulator ecotype of Sedum alfredii; has been used to characterize the Cd flux in higher plants (Pineros NHE, non hyper accumulator ecotype of S. alfredii; PM, plasma membrane; SIET, et al., 1998; Ma et al., 2010; He et al., 2011; Li et al., 2012). How- scanning ion-selective electrode technique. ∗ ever, its application is limited to the roots (Pineros et al., 1998; Corresponding author at: Center for Research in Ecotoxicology and Environmen- He et al., 2011; Li et al., 2012) or suspension cells (Ma et al., 2010). tal Remediation, Agro-environmental Protection Institute, Ministry of Agriculture, Thus, SIET has not been fully applied in the monitoring of the spatial Tianjin 300191, PR China. Tel.: +86 22 23612822; fax: +86 22 23612823. E-mail address: [email protected] (R. Wang). characteristics of Cd transport. 0176-1617/$ – see front matter © 2012 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.jplph.2012.10.014 Author's personal copy 356 J. Sun et al. / Journal of Plant Physiology 170 (2013) 355–359 Fig. 1. Effect of CdCl2 (10 ␮M for 2 h) pre-exposure on the net Cd fluxes in different regions of the roots in hyperaccumulator (HE) and nonhyperaccumulator (NHE) Sedum 2+ alfredii. (a) Representative images showing the measuring positions and Cd flux profile in different regions, namely, the meristematic zone (region A), elongation zone (region B), mature zone (region C), and root hair cells (region D). The position and magnitude of the fluxes are indicated by arrows (black for HE and white for NHE); the arrows directed toward the root indicate influx, whereas those directed away from the root denote efflux and (b) Mean rates of Cd fluxes in the different regions. Each column represents the mean of four individual plants. At least two roots in each plant or two root hair cells in each root were measured. The bars represent the standard error of the mean. Columns labeled with a and b indicate a significant difference at P < 0.05. ◦ ◦ The Cd/zinc (Zn) hyperaccumulating plant species S. alfredii temperatures ranging from 20 C to 25 C and with a 16 h photope- remarkably tolerates and hyperaccumulates Cd in its leaves. Thus, riod and relative air humidity of 70%/85%. The nutrient solution it is a useful model for the study of Cd transport and hyperaccumu- was continuously aerated and renewed every 48 h. Seedlings with lation in plants (Yang et al., 2004; Lu et al., 2008, 2009, 2010; Lu, uniform roots (approximately 3–4 cm) were selected for the SIET 2008; Tian et al., 2011). In this study, a Cd-selective microelectrode experiments. was used to compare the Cd fluxes in the different cell types of HE and NHE S. alfredii, including the meristematic, elongation, and Isolation of mesophyll protoplasts mature zones of the roots, as well as the root hair cells, vascular bundles in the leaf petiole, mesophyll tissues, isolated mesophyll Mesophyll protoplasts were isolated from the epidermis- protoplasts, and intact vacuoles. The results suggest that the non- removed leaves of the two ecotypes. The mesophyll tissues invasive microelectrode is a highly effective tool that exhibits a high were incubated in a cell wall-digesting medium consist- degree of spatial resolution in the study of the Cd transport at the ing of a mannitol medium [500 mM mannitol, 10 mM 2-(N- tissue, cellular, and sub-cellular levels in plants. morpholino)ethanesulfonic acid (MES), and 10 ␮M CaCl2, pH 5.5], 1.5% cellulase Onozuka R-10 (Yakult Honsha), 1% cellulysin (Cal- ◦ Materials and methods Biochem), and 0.1% pectolyase Y-23 (Yakult Honsha) for 4 h at 28 C. The protoplasts were then collected by filtration through a nylon Plant materials mesh and further purified by gradient centrifugation (Cosio et al., 2004). The protoplasts were kept shortly in test tubes with ice prior The spatial characteristics and real-time kinetics of Cd transport to the SIET experiments. were investigated using Sedum alfredii, a Cd/Zn-hyperaccumulating plant native to China. S. alfredii HE and NHE with healthy and SIET uniform shoots were selected and pre-cultured for 2 weeks in a basic nutrient solution for rooting according to a previously Net fluxes of Cd were noninvasively measured using SIET (BIO- reported method (Yang et al., 2004). The pH of the nutrient solution 001A; Younger USA, LLC, MA, USA) (Sun et al., 2009, 2010; Ma was adjusted daily to 5.5 using sodium hydroxide or hydrochlo- et al., 2010; He et al., 2011; Li et al., 2012). More details about this ric acid. The plants were grown under greenhouse conditions at technique are provided in Supplemental method. Author's personal copy J. Sun et al. / Journal of Plant Physiology 170 (2013) 355–359 357 Experimental protocols Steady-state Cd flux recording The roots of intact HE and NHE seedlings were exposed to a 10 ␮M CdCl2 for 2 h, rinsed with redistilled water, immediately immobilized in the measuring solution (10 ␮M CdCl2, 50 ␮M CaCl2, pH 5.5), and then equilibrated for 10 min (Pineros et al., 1998).
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