Abstract
The subcellular distribution of chromium in Leersia hexandra Swartz, a Cr-accumulating plant found in China, was studied by differential centrifugation, transmission electron microscope and energy dispersive analysis of X-ray. Subcellular fractionation of Cr-containing tissues showed that most of the accumulated Cr was isolated to the cell walls in roots and the vacuoles in leaves. When the plant was grown in a nutrient solution containing 60 mg L−1 Cr, 83.2% of the root Cr was localized in the cell wall fraction, while 57.5% of leaf Cr was localized in the vacuole and cytoplasm fraction. Transmission electron microscopic analysis revealed that those cell compartments contained especially electron dense areas. Energy dispersive X-ray spectra showed the electron dense areas contained high Cr. However, the dark electron precipitates were never observed in the plant cells without Cr treatment. In all treatment groups (5, 30 and 60 mg L−1), the fraction containing the lowest level of Cr was the organelle fraction in roots as well as leaves. These results indicated that Cr accumulated in the L. hexandra was preferentially stored in the cell walls of roots and the vacuoles of leaves. This phenomenon diverted Cr ions from metabolically active compartment (chloroplast, mitochondria), resulting in a reduction of Cr toxicity in the plant cell.
Similar content being viewed by others
Abbreviations
- TEM:
-
transmission electron microscope
- AAS:
-
flame atomic absorption spectrophotometer
- EDX:
-
energy dispersive analysis of X-ray
- DW:
-
dry weight
- F w :
-
cell wall fraction
- F o :
-
organelle fraction
- F v :
-
cytoplasm and vacuole fraction
- LSD:
-
Fisher’s least significant difference
References
Allen DL, Jarrell WM (1989) Proton and copper adsorption to maize and soybean root cell walls. Plant Physiol 89:823–832 doi:10.1104/pp.89.3.823
Appenroth KJ, Bischoff M, Gabrys H, Stoeckel J, Swartz H, Walckzak T, Winnefeld K (2000) Kinetics of chromium formation and reduction in fronds of the duckweed Spirodela polyrhiza-a low frequency EPR study. J Inorg Biochem 78:235–242 doi:10.1016/S0162-0134(00)00018-0
Bidwell SD, Crawford SA, Woodrow IE, Sommer-Knudsen J, Marsshall AT (2004) Sub-cellular localization of Ni in the hyperaccumulator, Hybanthus floribundus (Lindley) F. Muell. Plant Cell Environ 27:705–716 doi:10.1111/j.0016-8025.2003.01170.x
Bonet A, Poschenrieder C, Barceló J (1991) Chromium III-iron interaction in Fe-deficient and Fe-sufficient bean plants. I Growth and nutrient content. J Plant Nutr 14:403–414 doi:10.1080/01904169109364211
Carrier P, Baryla A, Havaux M (2003) Cadmium distribution and microlo-calization (Brassica napus) in oilseed rape after long-term growth on cadmium contaminated soil. Planta 216:939–950
Chatterjee J, Chatterjee C (2000) Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ Pollut 109:69–74 doi:10.1016/S0269-7491(99)00238-9
Chen T, Yan X, Liao X, Xiao X, Huang Z, Xie H, Zhai L (2005) Subcellular distribution and compartmentalization of arsenic in Pteris vittata L. Chin Sci Bull 50(24):2843–2849
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719 doi:10.1016/j.biochi.2006.07.003
Clemens S, Palmgren MG, Krämer U (2002) A long way ahead understanding and engineering plant metal accumulation. Trends Plant Sci 7(7):309–315 doi:10.1016/S1360-1385(02)02295-1
Davies FT, Puryear JD, Newton RJ, Egilla JN, Grossi JAS (2002) Mycorrhizal fungi increase chromium uptake by sunflower plants: influence on tissue mineral concentration, growth, and gas exchange. J Plant Nutr 25:2389–2407 doi:10.1081/PLN-120014702
Gardea-Torresdey JL, Rosa G, Peralta-Videa JR, Montes M, Cruz-Jimenez G, Cano-Aguilera I (2005) Differential uptake and transport of trivalent and hexavalent chromium by tumbleweed (Salsola kali). Arch Environ Contam Toxicol 48:225–232 doi:10.1007/s00244-003-0162-x
Hauschild MZ (1993) Putrescine (1,4-diaminobutane) as an indicator of pollution- induced stress in higher plants: Barley and rape stressed with Cr(III) or Cr(VI). Ecotoxicol Environ Saf 26:228–247 doi:10.1006/eesa.1993.1052
Hayens RJ (1980) Ion exchange properties of roots and ionic interactions within the root apoplasm: Their role in ion accumulation by plants. Bot Rev 46:75–99 doi:10.1007/BF02860867
Ke W, Xiong Z, Xie M, Luo Q (2007) Accumulation, subcellular localization and ecophysiological responses to copper stress in two Daucus carota L. populations. Plant Soil 292:291–304 doi:10.1007/s11104-007-9229-1
Krämer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol 122:1343–1353 doi:10.1104/pp.122.4.1343
Lai Y, Wang Q, Yang L, Huang B (2006) Subcellular distribution of rare earth elements and characterization of their binding species in a newly discovered hyperaccumulator Pronephrium simplex. Talanta 70:26–31 doi:10.1016/j.talanta.2005.12.062
Li TQ, Yang XE, Yang JY, He ZL (2006) Zn accumulation and subcellular distribution in the Zn hyperaccumulator Sedum alfredii Hance. Pedospere 16(5):616–623 doi:10.1016/S1002-0160(06)60095-7
Lombi E, Zhao FJ, Fuhrmann M, Ma LQ, McGrath SP (2002) Arsenic distribution and speciation in the fronds of the hyperaccumulator Pteris vittata. New Phytol 156:195–203 doi:10.1046/j.1469-8137.2002.00512.x
Lytle CM, Lytle FW, Yang N, Qian JH, Hansen D, Zayed A, Terry N (1998) Reduction of Cr(VI) to Cr(III) by wetland plants: potential for in situ heavy metal detoxification. Environ Sci Technol 32(20):3087–3093 doi:10.1021/es980089x
Mishra S, Shanker K, Srivastava MM, Srivastava S, Shrivastav R, Dass S, Prakash S (1997) A study on the uptake of trivalent and hexavalent chromium by paddy (Oryza sativa): possible chemical modifications in rhizosphere. Agric Ecosyst Environ 62:53–58 doi:10.1016/S0167-8809(96)01105-X
Ni C, Chen Y, Lin Q, Tian G (2005) Subcellular localization of copper in tolerant and non tolerant plant. J Environ Sci (China) 17(3):452–456
Poschenrieder C, Vazquez MD, Bonet A, Barceló J (1991) Chromium III-iron interaction in Fe-deficient and Fe-sufficient bean plants. II Ultrastructural aspects. J Plant Nutr 14:415–428 doi:10.1080/01904169109364212
Samantaray S, Rout GR, Das P (1998) Role of chromium on plant growth and metabolism. Acta Physiol Plant 20(2):201–212 doi:10.1007/s11738-998-0015-3
Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753 doi:10.1016/j.envint.2005.02.003
Sharma DC, Sharma CP, Tripathi RD (2003) Phytotoxic lesions of chromium in maize. Chemosphere 51:63–68 doi:10.1016/S0045-6535(01)00325-3
Skeffington RA, Shewry PR, Petersen PJ (1976) Chromium uptake and transport in barley seedlings Hordeum vulgare. Planta 132:209–214 doi:10.1007/BF00399719
Vazquez MD, Poschenrieder C, Barceló J (1987) Chromium VI induced structural and ultrastructural changes in bush bean plants (Phaseolus vulgaris L). Ann Bot (Lond) 59:427–438
Vazquez MD, Poschenrieder C, Barceló J (1992) Ultrastructural effects and localization of low cadmium concentrations in bean roots. New Phytol 120:215–226 doi:10.1111/j.1469-8137.1992.tb05657.x
Wallace A, Soufi SM, Cha W, Romney E (1976) Some effects of chromium toxicity on bush bean plants grown in soil. Plant Soil 44:471–473 doi:10.1007/BF00015901
Wu FB, Dong J, Qian QQ, Zhang GP (2005) Subcellular distribution and chemical form of Cd and Cd-Zn interaction in different barley genotypes. Chemosphere 60:1437–1446 doi:10.1016/j.chemosphere.2005.01.071
Zayed A, Terry N (2003) Chromium in the environment: factors affecting biological remediation. Plant Soil 249:139–156 doi:10.1023/A:1022504826342
Zhang XH, Liu J, Huang HT, Chen J, Zhu YN, Wang DQ (2007) Chromium accumulation by the hyperaccumulator plant Leersia hexandra Swartz. Chemosphere 67:1138–1143 doi:10.1016/j.chemosphere.2006.11.014
Acknowledgements
The authors thank the financial supports from the Scientific Research and Technological Development Project of Guangxi (GuiKeGong 0816003-1-1), the Natural Science Foundation of China (30760049, 40663002, 20665003) and the Provincial Natural Science Foundation of Guangxi (GuiKeNeng 0701K005, GuiKeZi 0728222). Financial assistance for this research was also provided through the Program to Sponsor Teams for Innovation in the Construction of Talent Highlands in Guangxi (GuiKeRen 2007-71, 2004217). Two anonymous reviewers are thanked for their cogent reviews of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Juan Barcelo.
Rights and permissions
About this article
Cite this article
Liu, J., Duan, CQ., Zhang, XH. et al. Subcellular distribution of chromium in accumulating plant Leersia hexandra Swartz. Plant Soil 322, 187–195 (2009). https://doi.org/10.1007/s11104-009-9907-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-009-9907-2