Abstract
Translocation of cadmium (Cd) in the tissues of Vicia faba, the water content in biomass, the biomass production, and the glutathione and phytochelatin tissue concentrations were studied and correlated with the plant sensitivity and/or tolerance to Cd. The total concentrations of Cd were determined by inductively coupled plasma/mass spectrometry (ICP-MS), the concentrations of glutathione (GSH) and phytochelatins 2 and 3 (PC2 and PC3) were determined by on-line high performance liquid chromatography/electrospray-ionization tandem mass spectrometry (HPLC–ESI–MS–MS) in the roots and leaves of the sensitive and the tolerant cultivars of V. faba grown in Cd containing nutrient solutions (NS, 0–100 μmol l−1 Cd2+). Both the cultivars of V. faba accumulate a major portion of Cd in the roots and only a minor part of ca. 4% in the leaves. The differences between the cultivars concerning Cd accumulation in leaves were apparent from higher Cd concentrations in NS and the Cd amount in the sensitive cultivar was approximately twice as high. In the roots, the differences between the cultivars in the Cd accumulation were only statistically significant with the highest Cd concentrations in NS, with the tolerant cultivar accumulating about 16% more of Cd compared to the sensitive one. The biomass production of the sensitive cultivar decreased approximately twice as fast with increasing Cd concentration in NS. The biomass water content decreased with increasing Cd concentration in NS in both the cultivars. In general, the GSH concentration did not linearly correlate with Cd accumulation, except for the roots of the sensitive cultivar where it was independent, and was higher in the sensitive cultivar than in the tolerant one in both the leaves and roots. The GSH concentration in leaves was approximately one order of magnitude higher than that in the roots for both the cultivars. The relationships between the PC and Cd concentrations in tissues were found nonlinear. At lower Cd accumulation levels, the PC concentrations followed an increase in the Cd accumulation in both the roots and leaves, whereas at higher Cd accumulations the relations differed between roots and leaves. In the roots, the PC concentrations decreased with increasing Cd accumulation, whereas the PC concentration in the leaves followed the decrease in the Cd accumulation.
Similar content being viewed by others
Abbreviations
- Cd:
-
Cadmium
- C Cd-leaves :
-
Cd concentration in the leaves
- C Cd-NS :
-
Cd concentration in the nutrient solution
- C Cd-roots :
-
Cd concentration in the roots
- DW:
-
Dry weight
- FW:
-
Fresh weight
- GSH:
-
Glutathione, γ-Glu-Cys-Gly
- HPLC–ESI–MS–MS:
-
High performance liquid chromatography electrospray-ionization tandem mass spectrometry
- ICP-MS:
-
Inductively coupled plasma/mass spectrometry
- MTs:
-
Metallothioneins
- NS:
-
Nutrient solution
- PC, PCs:
-
Phytochelatin, phytochelatins
- PC2:
-
Phytochelatin 2 (γ-Glu-Cys)2-Gly
- PC3:
-
Phytochelatin 3 (γ-Glu-Cys)3-Gly
- R :
-
Correlation coefficient
References
Adriano DC (1986) Trace elements in the terrestrial environment. Springer, New York
Beck A, Lendzian K, Oven M, Christmann A, Grill E (2003) Phytochelatin synthase catalyzes key step in turnover of glutathione conjugates. Phytochemistry 62:423–431
Béraud E, Cotelle S, Leroy P, Férard JF (2007) Genotoxic effects and induction of phytochelatins in the presence of Cd in Vicia faba roots. Mutat Res 633:112–116
Cabrera C, Ortega E, Lorenzo ML, Lopez MC (1998) Cd contamination of vegetable crops, farmlands, and irrigation waters. Rev Environ Contam Toxicol 154:55–81
Cataldo DA, Garland TR, Wildung RE (1981) Cd uptake kinetics in intact soybean plants. Plant Physiol 68:835–839
Cieslinski G, Nielsen GH, Hogue EJ (1996) Low-molecular-weight organic acids in rhizosphere soils of durum wheat and their effect on Cd bioaccumulation. Plant Soil 180:267–276
Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832
Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to Cd in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot 52:1101–1109
Ederli L, Reale L, Ferranti F, Pasqualini S (2004) Responses induced by high concentration of Cd in Phragmites australis roots. Physiol Plant 121:66–74
El Zohri M, Čabala R, Frank H (2005) Quantification of phytochelatins in plants by reversed-phase HPLC–ESI–MS–MS. Anal Bioanal Chem 382:1871–1876
Gorinova N, Nedkovska M, Todorovska E, Simova-Stoilova L, Stoyanova Z, Georgieva K, Demirevska-Kepova K, Atanasov A, Herzig R (2007) Improved phytoaccumulation of Cd by genetically modified tobacco plants (Nicotiana tabacum L.). Physiological and biochemical response of the transformants to Cd toxicity. Environ Pollut 145:161–170
Greger M, Brammer E, Lindberg S, Larsson G, Idestam-Almquist J (1991) Uptake and physiological effects of Cd in sugar beet (Beta vulgaris) related to mineral provision. J Exp Bot 42:729–737
Haag-Kerwer A, Schäfe HJ, Heiss S, Walter C, Rausch T (1999) Cd exposure in Brassica juncea caused a decline in transpiration rate and leaf expansion without effect on photosynthesis. J Exp Bot 50:1827–1835
Hart JJ, Welch RM, Norvell WA, Sullivan LA, Kochian LV (1998) Characterization of Cd binding, uptake, and translocation in intact seedlings of bread and durum wheat cultivars. Plant Physiol 116:1413–1420
Hernández LE, Cooke DT (1997) Modification of the root plasma membrane lipid composition of Cd treated Pisum sativum. J Exp Bot 48:1375–1381
Howden R, Goldsborough PB, Andersen CD, Cobett CS (1995) Cd-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol 107:1059–1066
Jones JRE (1939) The relation between the electrolytic solution pressures of the metals and their toxicity to the stickleback (Gasterosteus aculeatus L.). J Exp Biol 16:425–437
Kabata-Pendias A, Pendias H (1992) Trace elements in soils and plants, 2nd edn. CRC Press, Boca Raton
Knecht JA, van Dillen M, Koevoets PLM, Schat H, Verkeij JAC, Ernst WHO (1994) Phytochelatins in Cd-sensitive and Cd-tolerant Silene vulgaris. Plant Physiol 104:255–261
Landberg T, Greger M (2004) No phytochelatin (PC2 and PC3) detected in Salix viminalis. Physiol Plant 121:481–487
Li YM, Chaney RL, Schneiter AA, Miller JF (1995) Screening for low grain Cd phenotypes in sunflower, durum wheat and flax. Crop Sci 35:137–141
Liu WJ, Zhu YG, Smith FA, Smith SE (2004) Do iron plaque and genotypes affect arsenate uptake and translocation by rice seedlings (Oryza sativa L.) grown in solution culture? J Exp Bot 55:1707–1713
Liu CP, Shen ZG, Li XD (2007) Accumulation and detoxification of Cd in Brassica pekinensis and B. chinensis. Biol Plant 51:116–120
Loscos J, Naya L, Ramos J, Clemente MR, Matamoros MA, Becana M (2006) A reassessment of substrate specificity and activation of phytochelatin synthases from model plants by physiologically relevant metals. Plant Physiol 140:1213–1221
Lozano-Rodriguez E, Hernandez LE, Bonay P, Carpena-Riuz RO (1997) Distribution of Cd in shoot and root tissues of maize and pea plants: physiological disturbances. J Exp Bot 48:123–128
Maier EA, Matthews RD, McDowell JA, Walden RR, Ahner BA (2003) Environmental Cd levels increase phytochelatin and glutathione in lettuce grown in a chelator-buffered nutrient solution. J Environ Qual 32:1356–1364
Martinka M, Lux A (2006) Intraspecific variation of Silene dioica L. in uptake and translocation of Cd related to endodermal development. In: Teixeira da Silva JA (ed) Floriculture, ornamental and plant biotechnology. Advances and topical issues, vol III, 1st ed. edn. GSB, UK, pp 312–316
Mathys W (1973) Vergleichende Untersuchungen der Zinkaufnahme von resistent und sensitiven Populationen von Agrostis tenuis Sibth. Flora Jena 162:492–499
Mathys W (1975) Enzymes of heavy metal-resistant and nonresistant populations of Silene cucubalus and their interactions with some heavy metals in vitro and in vivo. Physiol Plant 33:161–165
Meister A (1995) Glutathione biosynthesis and its inhibition. Method Enzymol 251:3–7
Noctor G, Strohm M, Jouanin L, Kunert KJ, Foyer CH, Rennenberg H (1996) Synthesis of glutathione in leaves of transgenic poplar overexpressing γ-glutamylcysteine synthetase. Plant Physiol 11:1071–1078
Noctor G, Arisi ACM, Jouanin L, Kunert KJ, Rennenberg H, Foyer CH (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49:623–647
Oven M, Raith K, Neubert RHH, Kutchan TM, Zenk MH (2001) Homo-phytochelatins are synthesized in response to Cd in azuky beans. Plant Physiol 126:1275–1280
Penner GA, Clark J, Bezte LZ, Lisle D (1995) Identification of RAPD markers linked to a gene governing Cd uptake in durum wheat. Genome 38:543–547
Persson DP, Hansen TH, Holm PE, Schjoerring JK, Hansen HCB, Nielsen J, Cakmak I, Husted S (2006) Multi-elemental speciation analysis of barley genotypes differing in tolerance to Cd toxicity using SEC-ICP-MS and ESI-TOF-MS. J Anal Atom Spectrom 21:996–1005
Pomponi M, Censi V, Di Girolamo V, De Paolis A, Sanita di Toppi L, Aromolo R, Costantino P, Cardarelli M (2006) Overexpression of Arabidopsis phytochelatin synthase in tobaco plants enhances Cd2+ tolerance and accumulation but not translocation to the shoot. Planta 223:180–190
Poschenrieder C, Gunsé B, Barceló J (1989) Influence of Cd on water relations, stomatal resistance, and abscisic acid content in expanding bean leaves. J Plant Physiol 90:1365–1371
Ramos J, Clemente MR, Naya L, Loscos J, Pérez-Rentomé C, Sato S, Tabata S, Becana M (2007) Phytochelatin synthases of the model legume Lotus japonicus. A small multigene family with differential response to Cd and alternatively spliced variants. Plant Physiol 143:1110–1118
Ric De Voss CHR, Vonk MJ, Vooijs R, Schat H (1992) Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol 98:853–858
Rodecap KD, Tingey DT, Tibbs JH (1981) Cd-induced ethylene production in bean plant. Z Pflanzenphysiol 105:65–74
Ruegsegger A, Brunold C (1992) Effect of Cd on ‘y-glutamylcysteine synthesis in maize seedlings. Plant Physiol 99:428–433
Sanita di Toppi L, Gabbrielli R (1999) Response to Cd in higher plants. Environ Exp Bot 41:105–130
Slováková L, Klecová-Šimonová E, Henselová M, Hudák J (2007) Antioxidant enzymes of tolerant (Brassica juncea L.) and susceptible [Vigna radiata (L.) Wilczek] plants to Cd. In: Bláha L (ed) Influence of abiotic and biotic stressors to property of plants 2007. Proceedings VÚRV v.v.i., Prague-Ruzyne, pp 355–362
Sriprang R, Hayashi M, Ono H, Takagi M, Hirata K, Murooka Y (2003) Enhanced accumulation of Cd2+ by a Mesorhizobium sp. transformed with a gene from Arabidopsis thaliana coding for phytochelatin synthase. Appl Environ Microbiol 69:1791–1796
Srivastava S, Tripathi RD, Dwivedi UN (2004) Synthesis of phytochelatins and modulation of antioxidants in response to Cd stress in Cuscuta reflexa—an angiospermic parasite. J Plant Physiol 161:665–674
Steffens JC (1990) The heavy metal-binding peptides of plants. Annu Rev Plant Mol Biol 41:553–575
Sun Q, Wang XR, Ding SM, Yuan XF (2005) Effects of interaction between Cd and plumbum on phytochelatins and glutathione production in wheat (Triticum aestivum L.). J Integr Plant Biol (Acta Bot Sin) 47:435–442
Szalai G, Janda T, Galan-Goldhirsh A, Páldi E (2002) Effect of Cd treatment on phytochelatin synthesis in maize. Acta Biol Szeged 46:121–122
Tsyganov VE, Belimov AA, Borisov AY, Safronova VI, Georgi M, Dietz KJ, Tikhonovich IA (2007) A chemically induced new pea (Pisum sativum) mutant SGECdt with increased tolerance to, and accumulation of, Cd. Ann Bot 99:227–237
Van Bruwaene R, Kirchmann R, Impens R (1984) Cd contamination in agriculture and zootechnology. Experientia 40:43–52
Vatamaniuk OK, Mari S, Lu YP, Rea PA (2000) Mechanism of heavy metal ion activation of phytochelatin (PC) synthase. J Biol Chem 275:31451–31459
Vázqez S, Goldsbrough P, Carpena RO (2009) Comparative analysis of the contribution of phytochelatins to Cd and arsenic tolerance in soybean and white lupin. Plant Physiol Biochem 47:63–67
Villalobos-Pietrini R, Flores-Marquez AR, Gomez-Arroyo S (1994) Cytogenetic effects in Vicia faba of the polluted water from rivers of the Tlaxcala hydrological system, Mexico. Rev Int Contam Ambient 10:83–88
Yen TY, Villa JA, DeWitt JG (1999) Analysis of phytochelatin–Cd 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
Zhao FJ, Hamon RE, Lombi E, McLaughlin MJ, McGrath SP (2002) Characteristics of Cd uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 53:535–543
Acknowledgments
R. Čabala would like to acknowledge the research project VZ MSM 0021620857 from the Ministry of Education, Youth and Sports of the Czech Republic. L’. Slováková gratefully acknowledges a partial financial support from the grants of the Slovak grant agencies VEGA No. 1/4354/07, COST 0004-06 APVV.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. Ueda.
Rights and permissions
About this article
Cite this article
Čabala, R., Slováková, L., El Zohri, M. et al. Accumulation and translocation of Cd metal and the Cd-induced production of glutathione and phytochelatins in Vicia faba L.. Acta Physiol Plant 33, 1239–1248 (2011). https://doi.org/10.1007/s11738-010-0653-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11738-010-0653-0