Effects of cadmium in plants of Sphagneticola trilobata (L.) Pruski
Keywords:
Glutathione, oxidative stress, phytochelatins, phytoremediation, tolerant plants, wedeliaAbstract
Cadmium (Cd2+) is a pollutant of great environmental concern due to its multiple origins (natural and anthropogenic), the ability to accumulate in organs and tissues, and the deleterious effects it can cause in organisms. In the present study, we investigated the effects of Cd2+ exposure on Sphagneticola trilobata plants. We evaluated the accumulation of Cd2+, the plant biomass, the content of chlorophyll, soluble sugars, proteins and the production of malondialdehyde and thiols as markers of oxidative stress and tolerance, respectively. The Cd2+ content in the plant organs increased proportionally to the concentration of CdCl2 in the environment, reaching accumulatively 1306, 193 and 52 mg·kg-1 in roots, stems and leaves, respectively. Some toxic effects such as a decrease in the root biomass, alterations in the polypeptide pattern of the leaves, reduction in the chlorophyll content, and an increase in the amount of malondialdehyde was observed at higher concentrations of CdCl2. An increase in the content of soluble sugars was also seen, which are markers of tolerance associated with a protection mechanism against the oxidative stress. In addition, an increase on heavy metals chelating thiols such as L-cysteine, glutathione and various phytochelatins was obtained in the plant roots. Our results demonstrated that S. trilobata is capable of accumulating Cd2+ and possesses tolerance mechanisms that make this plant an excellent option to be used for Cd2+ phytoremediation.
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References
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36. Ovecka, M. and T. Takac. 2014. Managing heavy metal toxicity stress in plants: biological and Biotechnological tools. Biotechnology Advances 32: 73-86.
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45. Sanita di Toppi, L. and R. Gabbrielli. 1999. Response to cadmium in higher plants. Environ Exp Bot 41: 105-130.
46. Sarwar, N., M. Imran, M. Shaheen, W. Ishaque, M. Asif Kamran and A. Matloob. 2017. Phytoremediation strategies for soils contaminated with heavy metals: Modifications and future perspectives. Chemosphere 171: 710¬-721.
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49. Singh, R., R.D. Tripathi, S. Dwivedi, M. Singh, P.K. Trivedi, D. Chakrabarty. 2010. Cadmium-induced biochemical responses of Vallisneria spiralis. Protoplasma. 245: 97-103.
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52. Solís-Domínguez, F.A., M.Z. Gonzalez-Chavez, R. Carrillo-Gonzalez and R. Rodriguez-Vazquez. 2007. Accumulation and localization of cadmium in Echinochloa polystachya grown within a hydroponic system. J Hazard Mater 141: 630-636.
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54. Su, D.C., W.P. Jiao, M. Zhou, X. Chen. 2010. Can Cadmium Uptake by Chinese Cabbage be Reduced After Growing Cd-Accumulating Rapeseed?. Pedosphere. 20(1): 90-95.
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56. Tamas, L., J. Dudıková, K. Durceková, L. Halusková, J. Huttová, I. Mistrık, M. Ollé. 2008. Alterations of the gene expression, lipid peroxidation, proline and thiol content along the barley root exposed to cadmium. J Plant Physiol. 165: 1193-1203.
57. Van den Ende, W. and R. Valluru. 2008. Sucrose, sucrosil oligosaccharides and oxidative stress: scavenging and salvaging? J Exp Bot 60: 9-18.
58. Verma, S. and R. Demey. 2001. Effect of cadmium on soluble sugars and enzymes on their metabolism in rice. Biol Plant 44: 117-123.
59. Wei, Z., L. Dong and Z. Tian. 2009. Fourier transform infrared spectrometry study on early stage of cadmium stress in clover leaves. Pak J Bot 41:1743–1750.
60. Wojcik, M., J. Vangronsveld and A. Tukiendorf. 2005. Cadmium tolerance in Thlaspi caerulescens: I. Growth parameters, metal accumulation and phytochelatin synthesis in response to cadmium. Environ Exp Bot. 53(2): 151-161.
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2. Akhter, M., C. Omelon, R. Gordon, D. Moser and S. Macfie. 2014. Localization and chemical speciation of cadmium in the roots of barley and lettuce. Environ Exp Bot. 100: 10-19.
3. Ali, H., E. Khan and M. Sajad. 2013. Phytoremediation of heavy metals. Concepts and applications. Chemosphere 91: 869-881.
4. Anjum, S., M. Tanveer, S. Tung, M. Anam, B. Shahzad and M. Hussain. 2016. Morpho-Physiological growth and yield responses of two contrasting maize cultivars to cadmium exposure. Clean-Soil Air Water 44: 29-36.
5. Brooks, R. 1998. Plants that hyperaccumulate heavy metals. Their role in phytoremediation, microbiology archaeology, mineral exploration and phytomining (CAB Intern). Wallingford.
6. Castrillo, M., 1999. Sucrose metabolism at three leaf development stages in bean plants Photosynthetica 36: 519-524.
7. Castrillo, M., B. Pernia, A. de Sousa and R. Reyes. 2012. Utilization of different aspects associated with cadmium tolerance in plants to compare sensitive and bioindicator species. In Anjum, N., et al (ed) Phytotechnologies remediation of environmental contaminants. Boca Raton-London. New York. CRC Press Taylor and Francis Group, Chapter 24, pp. 427-440.
8. Chaoui, A., S. Mazhoudi, M. Ghorbal and E. Ferjani. 1997. Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Sci 127: 139-147.
9. Cherif, J., N. Derbel, M. Nakkach, H. von Bergmann, F. Jemal, Z. Ben Lakhdar. 2011. Spectroscopic studies of photosynthetic responses of tomato plants to the interaction of zinc and cadmium toxicity. J Photochem Photobiol 111: 9-16.
10. Davidian, J. and S. Kopriva. 2010. Regulation of sulfate uptake and assimilation- the same or not the same?. Mol Plant 3: 314-325.
11. Deng, X., Y. Xia, W. Hu, H. Zhang and Z. Shen. 2010. Cadmium-induced oxidative damage and protective effects of N-acetyl-l-cysteine against cadmium toxicity in Solanum nigrum L. J. Hazard. Mat. 180: 722-729.
12. Fediuc, E., S. Lips, L. Erdei. 2005. O-acetylserine (thiol) lyase activity in Phragmites and Typha plants under cadmium and NaCl stress conditions and the involvement of ABA in the stress response. J Plant Physiol. 162: 865-872.
13. Fidalgo, F., R. Freitas, R. Ferreira, A.M. Pessoa and J. Teixeira. 2011. Solanum nigrum L. antioxidant defence system isozymes are regulated transcriptionally and posttranslationally in Cd-induced stress. Environ Exp Bot 72: 312-319.
14. Filek, M., J. Koscielniak, M. Labanowska, E. Bednarska and E. Bidzinskam. 2010. Selenium- induced protection of photosynthesis activity in rape (Brassica napus) seedlings subjected to cadmium stress. Fluorescence and EPR measurements. Photosynthesis Res 105: 27-37.
15. Fusconi, A., O. Repetto, E. Bona, N. Massa, C. Gallo, E. Dumas-Gaudot and G. Berta. 2010. Effects of cadmium on meristems activity and nucleus ploidy in roots of Pisum sativum L. cv Frisson seedlings. Environ Exp Bot 58: 253-260.
16. Gadapati, W. and S. Macfie. 2006. Phytochelatins are only partially correlated with Cd-stress in two species of Brassica. Plant Science. 170: 471-480.
17. Gallego, S., M. Kogan, C. Azpilicueta, C. Peña and M. Tomaro. 2005. Glutathione-mediated antioxidative mechanisms in sunflower (Helianthus annuus L.) cells in response to Cd stress. Plant Growth Regul. 46: 267-276.
18. Gallego, S., L. Peña, R. Barcia and C. Azpilicueta. 2012. Iannone M. Unravelling cadmium toxicity and tolerance in plants: Insight into regulatory mechanisms. Environ Exp Bot 83: 33-46.
19. Gill, S. and N. Tuteja. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bichem 48: 909-930.
20. Gratao, L., C. Monteiro, A. Antunes, L. Peres and R.A. Azevedo. 2008. Acquired tolerance of tomato (Lycopersicon esculentum cv. Micro-Tom) plants to cadmium-induced stress. Ann. Appl. Biol 153: 321-333.
21. Heath, R. and L. Packer. 1968. Photoperoxidation in isolated chloroplast. I. Kinetics and stoichometry of fatty acid peroxidation. Arch Biochem Biophys 125: 189-198.
22. Hossaim, Z. and S. Komatsu. 2013. Contribution of proteomic studies towards understanding plant heavy metal stress response. Front. Plant Sci 3: 310.
23. Hu, J., Y. Liu, G.X. Shi, F. Liang. 2009. The Responses of Sagittaria sagittifolia L. to Environmental Cadmium Stress. Journal of Wuhan Botanical Research. 27(2): 176-183.
24. Jia, Y., X. Ju, S. Liao, Z. Song and Z. Li. 2011. Phytochelatin synthesis in response to elevated CO2 under cadmium stress in Lolium perenne L. J Plant Physiol. 168: 1723-1728.
25. Jin, X., X. Yang, E. Islam, D. Liu and Q. Mahmood. 2008. Effects of cadmium on ultrastructure and antioxidative defense system in hyperaccumulator and non-hyperaccumulator ecotypes of Sedum alfredii Hance. J. Hazard. Mater. 156(1-3): 387-397.
26. Josefczak, M., T. Remans, J. Vangronsveld and A. Cuypers. 2012. Glutathione is a key player in metal-induced oxidative stress defenses. Int J Mol Sci 13: 3145–3175.
27. Keltjens, W.G. and M.L. Van Beusichem. 1998. Phytochelatins as biomarkers for heavy metal toxicity in maize: single metal effects of copper and cadmium. J. Plant Nutr. 21: 635-648.
28. Kováčik, J., B. Klejdus and M. Backor, 2009. Phenolic metabolism of Matricaria chamomilla plants exposed to nickel. J. Plant Physiol. 166: 1460-1464.
29. Lagriffoul, A., B. Mocquot, M. Mench and J. Vangronsveld. 1998. Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.). Plant Soil. 200: 241-250.
30. Laemmli, U. 1970. Cleavage of structural proteins during the assembly of the head of Bacteriophage T4. Nature 227: 680-685.
31. Lichtenthaler, H. 1987. Chlorophylls and carotenoids: pigments of photosynthetic Biomembranes. Method Enzymol 148: 350-382.
32. Lux, A., M. Martinka and M. Vaculik. 2011. White P. Root response to cadmium in the rhizosphere: a review. J Exp Bot 62: 21-37.
33. Meyer, J.Y. 2000. Preliminary review of the invasive plants in the Pacific islands (SPREP Member Countries). In: G. Sherley (ed.). Invasive Species in the Pacific: A Technical Review and Draft Regional Strategy. South Pacific Regional Environment Programme (SPREP). Apia, Samoa. pp 85-114.
34. Mishra, S., S. Srivastava, R.D. Tripathi, R. Govindarajan, S.V. Kuriakose and M.N.V. Prasad. 2006. Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol. Bioch. 44: 25-37.
35. Mohamed, A., A. Castagna, A. Ranieri, L. Sanita di Toppi. 2012. Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatins Biosynthesis. Plant Physiol Biochem 57: 15-22.
36. Ovecka, M. and T. Takac. 2014. Managing heavy metal toxicity stress in plants: biological and Biotechnological tools. Biotechnology Advances 32: 73-86.
37. Pallavi, J., C. Pradhan and A.B. Das. 2016. Effects of Cadmium Toxicity in Plants: A Review. Sch Acad J Biosc 4: 1074-1081.
38. Palma, J., G. Pastori, P. Bueno, S. Distefano and L. del Rio. 1997. Purification and properties of cytosolic copper, zinc superoxide dismutase from watermelon (Citrullus vulgaris Schrad.) cotyledons. Free radicals Res 26: 83-91.
39. Peng, Q., W. Chen, L. Wu and L. Bai. 2017. The Uptake, Accumulation, and toxic effects of cadmium in Barnyardgrass (Echinochloa crus-galli). Pol J Environ Stud 26: 779-784.
40. Pernía, B., A. de Souza, R. Reyes, M. Castrillo. 2008. Biomarkers of cadmium pollution in Plants. Interciencia 3: 112-119.
41. Rai, V., S. Khatoon, S.S. Bisht and S. Mehrotra. 2005. Effect of cadmium on growth, ultramorphology of leaf and secondary metabolites of Phyllanthus amarus Schum. and Thonn. Chemosphere. 61: 1644-1650.
42. Ranieri, A., A. Castagna, F. Scebba, M. Careri, I. Zagnoni, G. Predieri, M. Pagliari and L. Sanità di Toppi. 2005. Oxidative stress and phytochelatin characterisation in bread wheat exposed to cadmium excess. Plant Physiol. Bioch. 43: 45-54.
43. Rizwan, M., S. Ali, M. Idrees, H. Rizvi, M. Zia-ur-Rehman and F. Hanna. 2016. Cadmium stress in rice: toxic effects, tolerance mechanisms, and management: a critical review. Environ Sci Pollut Res 23: 17859-17879.
44. Sadi, B., A. Vonderheide, J.M. Gong, J.I. Schroeder, J.R. Shann and J.A. Caruso. 2008. An HPLC-ICP-MS technique for determination of cadmium phytochelatins in genetically modified Arabidopsis thaliana. J. Chromatography B. 861: 123-129.
45. Sanita di Toppi, L. and R. Gabbrielli. 1999. Response to cadmium in higher plants. Environ Exp Bot 41: 105-130.
46. Sarwar, N., M. Imran, M. Shaheen, W. Ishaque, M. Asif Kamran and A. Matloob. 2017. Phytoremediation strategies for soils contaminated with heavy metals: Modifications and future perspectives. Chemosphere 171: 710¬-721.
47. Shah, K., R.G. Kumar, S. Verma and R.S. Dubey. 2001. Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci. 161: 1135-1144.
48. Seth, C.S., P.K. Chaturvedi and V. Mishra. 2008. The role of phytochelatins and antioxidants in tolerance to Cd accumulation in Brassica juncea L. Ecotox. Environ. Saf. 71(1):76-85.
49. Singh, R., R.D. Tripathi, S. Dwivedi, M. Singh, P.K. Trivedi, D. Chakrabarty. 2010. Cadmium-induced biochemical responses of Vallisneria spiralis. Protoplasma. 245: 97-103.
50. Sneller, F.E.C., E.C.M. Noordover, W.M.T. Bookum, H. Schat, J.J.M. Bedaux and J.A.C. Verkleij. 1999. Quantitative Relationship between Phytochelatin Accumulation and Growth Inhibition during Prolonged Exposure to Cadmium in Silene vulgaris. Ecotoxicology. 8(3): 167-175.
51. Sneller, F., L. van Heerwaarden, P. Koevoets, R. Vooijs, H. Schat and J. Verkleij. 2000. Derivatization of Phytochelatins from Silene vulgaris, induced upon exposure to arsenate and cadmium: comparison of derivatization with Ellman´s reagent and monobromobimane. J Agric Food Chem 48: 4014-4019.
52. Solís-Domínguez, F.A., M.Z. Gonzalez-Chavez, R. Carrillo-Gonzalez and R. Rodriguez-Vazquez. 2007. Accumulation and localization of cadmium in Echinochloa polystachya grown within a hydroponic system. J Hazard Mater 141: 630-636.
53. Son, K., D. Kim, N. Koo and K. Kim. 2012. Detoxification through phytochelatin synthesis in Oenothera odorata exposed to Cd solutions. Environ Exp Bot 75: 9-15.
54. Su, D.C., W.P. Jiao, M. Zhou, X. Chen. 2010. Can Cadmium Uptake by Chinese Cabbage be Reduced After Growing Cd-Accumulating Rapeseed?. Pedosphere. 20(1): 90-95.
55. Sun, R.L., Q.X. Zhou, F.H. Sun and C.X. Jin. 2007. Antioxidative defense and proline/ phytochelatin accumulation in a newly discovered Cd-hyperaccumulator, Solanum nigrum L. Environ Exp Bot. 60(3): 468-476.
56. Tamas, L., J. Dudıková, K. Durceková, L. Halusková, J. Huttová, I. Mistrık, M. Ollé. 2008. Alterations of the gene expression, lipid peroxidation, proline and thiol content along the barley root exposed to cadmium. J Plant Physiol. 165: 1193-1203.
57. Van den Ende, W. and R. Valluru. 2008. Sucrose, sucrosil oligosaccharides and oxidative stress: scavenging and salvaging? J Exp Bot 60: 9-18.
58. Verma, S. and R. Demey. 2001. Effect of cadmium on soluble sugars and enzymes on their metabolism in rice. Biol Plant 44: 117-123.
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Published
2020-04-02
How to Cite
Pernía, B., Calabokis, M., Noris, K., Bubis, J., Guerra, M., & Castrillo, M. (2020). Effects of cadmium in plants of Sphagneticola trilobata (L.) Pruski. Bioagro, 31(2), 133-142. Retrieved from https://revistas.uclave.org/index.php/bioagro/article/view/2641
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