Abstract
The bioaccumulation efficiency of cadmium (Cd) by fenugreek (Trigonella foenum-graecum) was examined using different concentrations of CdCl2. The germination rate was similar to control except at 10 mM Cd. However, early seedling growth was quite sensitive to the metal from the lowest Cd level. Accordingly, amylase activity was reduced substantially on treatment of seeds with 0.5, 1, and 10 mM Cd. Cadmium also affected various other plant growth parameters. Its accumulation was markedly lower in shoots as compared to roots, reducing root biomass by almost 50 %. Plants treated with 1 and 5 mM Cd presented chlorosis due to a significant reduction in chlorophyll b especially. Furthermore, at Cd concentrations greater than 0.1 mM, plants showed several signs of oxidative stress; an enhancement in root hydrogen peroxide (H2O2) level and in shoot malondialdehyde (MDA) content was observed. Conversely, antioxidant enzyme activities (superoxide dismutase (SOD), ascorbate peroxidase (APX), and catalase (CAT)) increased in various plant parts. Likewise, total phenolic and flavonoid contents reached their highest values in the 0.5 mM Cd treatment, consistent with their roles in quenching low concentrations of reactive oxygen species (ROS). Consequently, maintaining oxidant and antioxidant balance may permit fenugreek to hyperaccumulate Cd and allow it to be employed in extremely Cd polluted soils for detoxification purposes.
Similar content being viewed by others
Abbreviations
- APX:
-
Ascorbate peroxidase
- CAT:
-
Catalase
- DTT:
-
Dithiothreitol
- E h :
-
Redox potential
- H2O2 :
-
Hydrogen peroxide
- MDA:
-
Malondialdehyde
- NBT:
-
Nitrobluetetrazolium
- ROS:
-
Reactive oxygen species
- SOD:
-
Superoxide dismutase
- TBA:
-
Thiobarbituric acid
- TCA:
-
Trichloroacetic acid
References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Asada K (1992) Ascorbate peroxidase: a hydrogen peroxide scavenging enzyme in plants. Physiol Plant 85:235–241
Baker AMJ, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biochemical resource for phytoremediation of metal polluted soil. In: Terry N, Banuelous G (eds) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, Florida, pp 85–107
Baryla A, Carrier P, Franck F, Coulomb C, Sahut C, Havaux M (2001) Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta 212:696–709
Beri V, Gupta R (2007) Acetylcholinesterase inhibitors neostigmine and physostigmine inhibit induction of alpha-amylase activity during seed germination in barley, Hordeum vulgare var. Jyoti. Life Sci 80:2386–2388
Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in condition. Anal Biochem 161:559–566
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72:248–254
Caspi V, Droppa M, Horvath G, Malkin S, Marder JB, Raskin VI (1999) The effect of copper on chlorophyll organization during greening of barley leaves. Photosynth Res 62:165–174
Chugh LK, Sawhney SK (1996) Effect of cadmium on germination, amylase and rate of respiration of germinating pea seeds. Environ Pollut 92:1–5
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719
De Oliveira LM, Ma LQ, Santos JAG, Guilherme LRG, Lessl JT (2014) Effects of arsenate, chromate, and sulfate on arsenic and chromium uptake and translocation by arsenic hyperaccumulator Pteris vittata L. Environ Pollut 184:187–192
Delmaila D, Labroussea P, Hourdina P, Larcherb L, Moeschb C, Botineaua M (2011) Physiological, anatomical and phenotypical effects of a cadmium stress in different-aged chlorophyllian organs of Myriophyllum alterniflorum DC (Haloragaceae). Environ Exp Bot 72:174–181
Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24
Di Salvatore M, Carafa AM, Carratù G (2008) Assessment of heavy metals phytotoxicity using seed germination and root elongation tests: a comparison of two growth substrates. Chemosphere 73:1461–1464
Dirk LMA, Krol AR, Vreugdenhil D, Hilhors WM, Bewley JD (1999) Galactomannan, soluble sugar and starch mobilization following germination of Trigonella foenum-graecum seeds. Plant Physiol Biochem 37:41–50
Epelde L, Jose MB, Javier HA, Barrutia O, Garbisu C (2008) Functional diversity as indicator of the recovery of soil health derived from Thlaspi caerulescens growth and metal phytoextraction. Appl Soil Ecol 39:299–310
Galfati I, Essaïd B, Beji-Sassi A, Abdallah H, Zaïer A (2011) Accumulation of heavy metals in native plants growing near the phosphate treatment industry, Tunisia, Carpath. J Earth Environ Sci 6:85–100
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Rev Plant Physiol Biochem 48:909–930
Hideaki S, Yasutake A, Hirashima T, Takamure Y, Kitano T, Waalkes MP (2008) Strain difference of cadmium accumulation by liver slices of inbred Wistar Imamichi and Fischer 344 rats. Toxicol in Vitro 22:338–343
Khemakhem B, Fendri I, Dahech I, Belguith K, Kammoun R, Mejdoub H (2012) Purification and characterization of a maltogenic amylase from Fenugreek (Trigonella foenum-graecum) seeds using the Box Benkhen Design (BBD). Ind Crop Prod 43:334–339
Kováčik J, Grúz J, Bačkor M, Tomko J, Strnad M, Repčák M (2008) Phenolic compounds composition and physiological attributes of Matricaria chamomilla grown in copper excess. Environ Exp Bot 62:145–152
Kumar N, Bauddha K, Kumar S, Dwivedi N, Singha DP, Barman SC (2013) Accumulation of metals in weed species grown on the soil contaminated with industrial waste and their phytoremediation potential. Ecol Eng 61:491–495
Lepp NW (1981) Effect of heavy metal pollution on plants. In Metal in the environment, App. Sci. Pub., London, UK. 2
Li W, Khan MA, Yamaguchi S, Kamiya Y (2005) Effects of heavy metals on seed germination and early seedling growth of Arabidopsis thaliana. Plant Growth Regul 46:45–50
Lian J, Zhouli L, Wei C, Xingyuan H (2011) Stimulative effect induced by low-concentration of cadmium in Lonicera japonica Thunb. Afr J Microbiol Res 6:826–833
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382
Lin R, Wang X, Luo Y, Du W, Guo H, Yin D (2007) Effects of soil cadmium on growth, oxidative stress and antioxidant system in wheat seedlings (Triticum aestivum L.). Chemosphere 69:89–98
Matsouka I, Beri D, Chinou I, Haralampidis C, Spyropoulos G (2011) Metals and selenium induce medicarpin accumulation and excretion from the roots of fenugreek seedling: a potential detoxification mechanism. Plant Soil 343:235–245
Mazid M, Khan TA, Mohammad F (2011) Role of secondary metabolites in defense mechanisms of plants. Biol Med 3:232–249
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugars. Anal Chem 31:426–428
Moussa H, Del-Gamal S (2010) Effect of salicylic acid pretreatment on cadmium toxicity in wheat. Biol Plant 54:315–320
Nadeem O, Kaakoush Mark R, George L (2008) Molecular responses of Campylobacter jejuni to cadmium stress. FEBS J 275:5021–5033
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Noa L, Amnon S, Oded Y, Elisha T (2001) The involvement of polyphenols and peroxidase activities in heavy-metal accumulation by epidermal glands of the waterlily (Nymphaeaceae). Planta 212:323–331
Pattnaik S, Reddy MV (2011) Accumulation and mobility of heavy metals in fenugreek (Trigonella foenum-graceum L.) and tomato (Lycopersicum esculentum Mill.) grown in the field amended with urban wastes, and their composts and vermicomposts. Int J Environ Manag 14:147
Perfus-Barbeoch L, Leonhardt N, Vavaddeur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32:539–548
Pinelo M, Rubilar M, Sineiro J, Nunez MJ (2004) Extraction on antioxidant phenolics from almond hulls (Prunus amygdalus) and pine sawdust (Pinus pinaster). Food Chem 85:267–273
Piotrowska-Niczyporuk A, Bajguz A, Bieta Zambrzycka E, Godlewska B (2012) Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). Plant Physiol Biochem 52:52–65
Piršelová B (2011) Monitoring the sensitivity of selected crops to lead, cadmium and arsenic. J Stress Physiol Biochem 7:3–38
Richards DE, King KE, Ait-ali T, Harberd NP (2001) How gibberellin regulates plant growth and development: a molecular genetic analysis of gibberellin signaling. Annu Rev Plant Physiol Plant Mol Biol 52:67–88
Robson TC, Braungardt CB, Rieuwerts J, Worsfold P (2014) Cadmium contamination of agricultural soils and crops resulting from sphalerite weathering. Environ Pollut 184:283–289
Romero-Puertas MC, Corpas FJ, Rodriguez-Serrano M, Gomez M, del Rio LA, Sandalio LM (2007) Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. J Plant Physiol 164:1346–1357
Salaskar D, Shrivastava M, Kale SP (2011) Bioremediation potential of spinach (Spinacia oleracea L.) for decontamination of cadmium in soil. Curr Sci 101:1359–1363
Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, Del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126
Schalscha E, Ahumada I (1998) Heavy metals in rivers and soils of central Chile. Water Sci Technol 37:251–255
Singh N, Ma LQ, Srivastava M, Rathina Sabapathi B (2006) Metabolic adaptations to arsenic-induced oxidative stress in Pteris vittata L. and Pteris ensiformis L. Plant Sci 170:274–282
Spyropoulos CG, Reid JSG (1985) Regulation of a-galactosidase activity and the hydrolysis of galactomannan in the endosperm of fenugreek (Trigonella foenum-graecum L.) seed. Planta 166:271–275
Tsiri D, Chinou I, Halabalaki M, Haralampidis K, Spyropoulos CG (2009) The origin of copper-induced medicarpin accumulation and its secretion from roots of young fenugreek seedlings are regulated by copper concentration. Plant Sci 176:367–374
Ute K (2010) Metal hyperaccumulation in plants. Rev Plant Biol 61:517–534
Van de Mortel JE, Schat H, Moerland PD, Loren V, van Themaat E, Van Der Ent S, Blankestijn H (2008) Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 31:301–324
Vig K, Megharaj M, Sethunathan N, Naidu R (2003) Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Adv Environ Res 8:121–135
Wang Y, Feng H, Qu Y, Cheng J, Zhao Z, Zhang M, Wang X, An L (2006) The relationship between reactive oxygen species and nitric oxide in ultraviolet-B-induced ethylene production in leaves of maize seedlings. Environ Exp Bot 57:51–61
Xu D, Chen Z, Sun K, Yan D, Kang M, Zhao Y (2013) Effect of cadmium on the physiological parameters and the subcellular cadmium localization in the potato (Solanum tuberosum L.). Ecotoxicol Environ Saf 97:147–153
Zhishen J, Mengcheng T, Jianming W (1999) Research on antioxidant activity of flavonoids from natural materials. Food Chem 64:555–559
Acknowledgments
This work was supported by grants from the Tunisian Ministry of Higher Education and Scientific Research. It was accomplished at Faculty of Sciences of Sfax. The authors gratefully acknowledge the support of Rania Ben Saâd and Imen Fendri for the helpful advice and Mohamed Ayedi for the technical assistance.
Conflict of interest
The authors disclose that there are no relationships or interests that could have direct or potential influence or impart bias on the work. The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Elena Maestri
Rights and permissions
About this article
Cite this article
Zayneb, C., Bassem, K., Zeineb, K. et al. Physiological responses of fenugreek seedlings and plants treated with cadmium. Environ Sci Pollut Res 22, 10679–10689 (2015). https://doi.org/10.1007/s11356-015-4270-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-4270-8