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Characteristics of cadmium accumulation and tolerance in Rorippa globosa (Turcz.) Thell., a species with some characteristics of cadmium hyperaccumulation

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Abstract

Characteristics of cadmium (Cd) accumulation and tolerance in Rorippa globosa (Turcz.) Thell., a species with some characteristics of cadmium hyperaccumulation were further investigated and compared with a closely related species, Rorippa islandica. The results showed that there was no phytotoxicity for R. globosa leaves or reduction in biomass when treated with 25 μg Cd g−1, although the concentration of Cd accumulated in the leaves was up to 218.9 μg Cd g−1 dry weight (DW). On the contrary, Cd toxicity was observed in R. islandica leaves by way of determining changes in fresh weight (FW), malondialdehyde (MDA) level and chlorophyll content while treated with 25 μg Cd g−1 DW. R. globosa had stronger self-protection ability than R. islandica to adapt to oxidative stress caused by Cd. Application of Cd significantly increased the activity of superoxide dismutase (SOD) in leaves, the activity of peroxidase (POD) in roots, and the activity of catalase (CAT) in leaves and roots of R. globosa. By contrast, in R. islandica, the activity of antioxidant enzymes was inhibited or unchanged by various Cd treatments. However, R. globosa leaves had higher activity of antioxidant enzymes such as SOD and POD than that of R. islandica. The antioxidative defense systems in R. globosa might play an important role in Cd tolerance. The Cd treatments significantly induced the synthesis of phytochelatins (PCs) in the two species. Leaf PCs and Cd accumulation by R. globosa were much greater than those by R. islandica, but root PCs and Cd accumulation by R. islandica were much greater than those by R. globosa, suggesting that PCs in leaves may be a biomarker of Cd hyperaccumulation, and the synthesis of PCs may be related to an increase in the uptake of Cd ions into the cytoplasm, not the primary mechanism for Cd tolerance.

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References

  • Assunçaõ AGL, Martins PD, De Folter S, Vooijs R, Schat H, Aarts MGM (2001) Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 24:217–226

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Baker AJM, McGrath SP, Sidoli CMD, Reeves RD (1994) The possibility of in situ heavy metal decontamination of polluted soils using crops of metal-accumulating plants. Res Conserv Recycl 11:41–49

    Article  Google Scholar 

  • Blinda A, Abou-Mandour A, Azarkovich M, Brune A, Dietz KJ (1996) Heavy metal-induced changes in peroxidase activity in leaves, roots and cell suspension cultures of Hordeum vulgare L. In: Obinger C, Burner U, Ebermann R, Penel C, Greppin H (eds) Plant peroxidases, biochemistry and physiology. University of Agriculture, Wien, pp 374–379

    Google Scholar 

  • Boominathan R, Doran PM (2003) Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyperaccumulator, Thlaspi caerulescens. Biotechnol Bioeng 83:158–167

    Article  CAS  PubMed  Google Scholar 

  • Brown SL, Chaney RL, Angle JS (1994) Phytoremediation potential of Thlaspi caerulescens and bladder campion for zinc-and cadmium-contaminated soil. J Environ Qual 23:1151–1157

    CAS  Google Scholar 

  • Brown SL, Chaney RL, Angle JS, Baker AJM (1995) Zinc and cadmium uptake by hyperaccumulator Thlaspi caerulescens grown in nutrient solution. Soil Sci Soc Am J 59:125–133

    Article  CAS  Google Scholar 

  • Cai Y, Braids O (2002) Biogeochemistry of environmentally important elements. ACS Symposium Series 835. American Chemical Society, Oxford University Press, Washington, DC

  • Chance B, Maehly AC (1955) Assay of catalases and peroxidases. In: Colowick SP, Kaplan NO (eds) Methods in enzymology. Academic Press, New York, pp 764–775

    Chapter  Google Scholar 

  • Chaney RL, Malik M, Li YM, Brown SL, Brewer EP, Angle JS, Baker AJM (1997) Phytoremediation of soil metals. Curr Opin Biotechnol 8:279–284

    Article  CAS  PubMed  Google Scholar 

  • Chaoui A, Mazhoudi S, Ghorbal MH, El Ferjani E (1997) Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzymes activities in bean (Phaseolus vulgaris L.). Plant Sci 127:139–147

    Article  CAS  Google Scholar 

  • Citterio S, Santagostino A, Fumagalli P, Prato N, Ranalli P, Sgorbati S (2003) Heavy metal tolerance and accumulation of Cd, Cr and Ni by Cannabis sativa L. Plant Soil 256:243–252

    Article  CAS  Google Scholar 

  • Cobbett CS (2000) Phytochelatin biosynthesis and function in heavy-metal detoxification. Curr Opin Plant Biol 3:211–216

    CAS  PubMed  Google Scholar 

  • Cosio C, Martinoia E, Keller C (2004) Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis halleri at the leaf cellular level. Plant Physiol 134:716–725

    Article  CAS  PubMed  Google Scholar 

  • Cosio C, DeSantis L, Frey B, Diallo S, Keller C (2005) Distribution of cadmium in leaves of Thlaspi caerulescens. J Exp Bot 56:765–775

    Article  CAS  PubMed  Google Scholar 

  • De Knecht JA, van Baren N, Ten Bookum WM, Sang HWWF, Koevoets PLM, Schat H, Verkleij JAC (1995) Synthesis and degradation of phytochelatins in cadmium-sensitive and cadmium-tolerant Silene vulgaris. Plant Sci 106:9–18

    Article  Google Scholar 

  • Ebbs S, Lau I, Ahner B, Kochian L (2002) Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens (J&C Presl.). Planta 214:635–640

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ 17:507–523

    Article  CAS  Google Scholar 

  • Frey B, Keller C, Zierold K, Schulin R (2000) Distribution of Zn in functionally different leaf epidermal cells of the hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 23:675–687

    Article  CAS  Google Scholar 

  • Garbisu C, Alkorta I (2001) Phytoextraction: a cost-effective plant-based technology for the removal of metals from the environment. Bioresource Technol 77:229–236

    Article  CAS  Google Scholar 

  • Gupta M, Tripathi RD, Rai UN, Chandra P (1998) Role of glutathione and phytochelatin in Hydrilla verticillata Royle and Vallisneria spiralis L. under mercury stress. Chemosphere 37:785–800

    Article  CAS  Google Scholar 

  • Havir EA, Brisson LF, Zelitch I (1996) Distribution of catalase isoforms in Nicotiana tabacum. Phytochemistry 41:699–702

    Article  CAS  Google Scholar 

  • Hegedüs A, Erdei S, Horváth G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci 160:1085–1093

    Article  PubMed  Google Scholar 

  • Keltjens WG, Van Beusichem ML (1998) Phytochelatins as biomarkers for heavy metal toxicity in maize and wheat: combined effects of copper and cadmium. Plant Soil 21:635–648

    CAS  Google Scholar 

  • Küpper H, Zhao FJ, McGrath SP (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119:305–311

    Article  Google Scholar 

  • Küpper H, Lombi E, Zhao FJ, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212:75–84

    Article  PubMed  Google Scholar 

  • Küpper H, Mijovilovich A, Meyer-Klaucke W, Kroneck PM (2004) Tissue- and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges Ecotype) revealed by X-ray absorption spectroscopy. Plant Physiol 134:748–757

    Article  PubMed  CAS  Google Scholar 

  • Lasat MM, Pence NS, Garvin DF, Ebbs SD, Kochian LV (2000) Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. J Exp Bot 51:71–79

    Article  CAS  PubMed  Google Scholar 

  • Lee MY, Shin HW (2003) Cadmium-induced changes in antioxidant enzymes from the marine alga Nannochloropsis oculata. J Appl Phycol 15:13–19

    Article  CAS  Google Scholar 

  • Liu PC, Wang H, Cheng JQ, Huang JC (2004a) Regulation of nitric oxide on drought-induced membrane lipid peroxidation in wheat leaves. Acta Bot Boreal Occident Sin 24:141–145

    CAS  Google Scholar 

  • Liu W, Shu WS, Lan CY (2004b) Viola baoshanensis, a plant that hyperaccumulates cadmium. Chin Bull Sci 49:29–32

    CAS  Google Scholar 

  • Liu MQ, Yanai J, Jiang RF, Zhang FS, McGrath SP, Zhao FJ (2008) Does cadmium play a physiological role in the hyperaccumulator Thlaspi caerulescens? Chemosphere 71:1276–1283

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Ueno D, Zhao FJ, McGrath SP (2005) Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 220:731–736

    Article  CAS  PubMed  Google Scholar 

  • Mocquot B, Vangronsvel DJ, Clijsters H, Mench M (1996) Copper toxicity in young maize (Zea mays L.) plants: effects on growth, mineral and chlorophyll contents, and enzyme activities. Plant Soil 82:287–300

    Google Scholar 

  • Morishirta T, Boratynski K (1992) Accumulation of Cd and other metals in organs of plants growing around metal smelters in Japan. Soil Sci Plant Nutr 38:781–785

    Google Scholar 

  • Navari-Izzo F, Quartacci MF (2001) Phytoremediation of metals: mechanisms against oxidative stress. Minerva Biotechnol 13:73–83

    Google Scholar 

  • Reeves RD (2003) Tropical hyperaccumulators of metals and their potential for phytoextraction. Plant Soil 249:57–65

    Article  CAS  Google Scholar 

  • Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 193–229

    Google Scholar 

  • Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668

    Article  CAS  PubMed  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2212

    CAS  PubMed  Google Scholar 

  • Sanità di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Article  Google Scholar 

  • Schat H, Llugany M, Vooijs R, Hartley-Whitaker J, Bleeker PM (2002) The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. J Exp Bot 53:2381–2392

    Article  CAS  PubMed  Google Scholar 

  • Shaw BP (1995) Effect of mercury and cadmium on the activities of antioxidative enzymes in the seedlings of Phaseolus aureus. Biol Plant 37:587–596

    Article  CAS  Google Scholar 

  • Somashekaraiah BV, Padmaja K, Prasad ARK (1992) Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): involvement of lipid peroxides in chlorophyll degradation. Physiol Plant 85:85–89

    Article  CAS  Google Scholar 

  • Srivastava M, Ma LQ, Singh N, Singh S (2005) Antioxidant responses of hyper-accumulator and sensitive fern species to arsenic. J Exp Bot 56:1335–1342

    Article  CAS  PubMed  Google Scholar 

  • Sun RL, Zhou QX, Sun FH, Jin CX (2007) Antioxidative defense and proline/phytochelatin accumulation in a newly-discovered Cd-hyperaccumulator, Solanum nigrum L. Environ Exp Bot 60:468–476

    Article  CAS  Google Scholar 

  • Uraguchi S, Watanabe I, Yoshitomi A, Kiyono M, Katsuji K (2006) Characteristics of cadmium accumulation and tolerance in novel Cd-accumulating crops, Avena strigosa and Crotalaria juncea. J Exp Bot 57:2955–2965

    Article  CAS  PubMed  Google Scholar 

  • Van Assche F, Clijsters H (1990) Effect of metal on enzyme activity in plants. Plant Cell Environ 13:195–206

    Article  Google Scholar 

  • Vitoria AP, Lea PJ, Azevedo RA (2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochemistry 57:701–710

    Article  CAS  PubMed  Google Scholar 

  • Wei SH, Zhou QX (2006) Phytoremdiation of cadmium-contaminated soils by Rorippa globosa using two-phase planting. Environ Sci Pollut Res 13:151–155

    Article  CAS  Google Scholar 

  • Wei CY, Chen TB, Huang ZC (2002) Cretan bake (Pteris cretica L.): an Arsenicaccumulating. Plant Acta Ecol Sin 22:777–782

    Google Scholar 

  • Wei SH, Zhou QX, Wang X, Zhang KS, Guo GL (2004) A newly-found Cd-hyperaccumulator Solanum nigrum L. Chin Bull Sci 49:2568–2573

    Google Scholar 

  • Wójcik M, Vangronsveld J, Tukiendorf A (2005) Cadmium tolerance in Thlaspi caerulescens I. Growth parameters, metal accumulation and phytochelatin synthesis in response to cadmium. Environ Exp Bot 53:151–161

    Google Scholar 

  • Wójcik M, Skórzyńska-Polit E, Ukiendorf A (2006) Organic acids accumulation and antioxidant enzyme activities in Thlaspi caerulescens under Zn and Cd stress. Plant Growth Regul 48:145–155

    Article  CAS  Google Scholar 

  • Wu YX, von Tiedemann A (2002) Impact of fungicides on active oxygen species and antioxidant enzymes in spring barley (Hordeum vulgare L.) exposed to ozone. Environ Pollut 116:37–47

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Long XX, Ye HB, He ZL, Stoffella PJ, Calvert DV (2004) Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259:181–189

    Article  CAS  Google Scholar 

  • Yen TY, Villa JA, DeWitt JG (1999) Analysis of phytochelatin-cadmium complexes from plant tissue culture using nano-electrospray ionization tandem mass spectrometry and capillary liquid chromatography/electrospray ionization tandem mass spectrometry. J Mass Spectrom 34:930–941

    Article  CAS  PubMed  Google Scholar 

  • Yurekli F, Porgali ZB (2006) The effects of excessive exposure to copper in bean plants. Acta Biol Cracov Bot 48:7–13

    Google Scholar 

  • Zenk MH (1996) Heavy metal detoxification in higher plants—a review. Gene 179:21–30

    Article  CAS  PubMed  Google Scholar 

  • Zhou QX, Song YF (2004) Principles and methods of contaminated soil remediation. Science Press, Beijing

    Google Scholar 

Download references

Acknowledgments

The research was financially supported by the Ministry of Science and Technology, People’s Republic of China as an 863 project (No. 2007AA061201), and by the Ministry of Education, People’s Republic of China as a grand fostering project (No. 707011), respectively.

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Correspondence to Qixing Zhou.

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Sun, R., Jin, C. & Zhou, Q. Characteristics of cadmium accumulation and tolerance in Rorippa globosa (Turcz.) Thell., a species with some characteristics of cadmium hyperaccumulation. Plant Growth Regul 61, 67–74 (2010). https://doi.org/10.1007/s10725-010-9451-3

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