Arsenic bioaccumulation and tolerance in terrestrial fern Ampelopteris prolifera (Retz.) Copel and aquatic fern, Azolla pinnata R. Br. are related to coordinated but differential responses of their antioxidant defense components
Authors/Creators
- 1. Plant Cell & Stress Biology Lab, Department of Botany, R.P.M. College (University of Calcutta), Uttarpara, 712258, West Bengal, India
Description
ABSTRACT
Present study aims to analyze the arsenate bioaccumulation and antioxidant defense responses in fronds of terrestrial fern Ampelopteris prolifera (Retz.) Copel and an aquatic fern Azolla pinnata R. Br. Both the ferns were exposed to increased concentrations of sodium arsenate (As; 0, 20, 60, 100, and 160 mg L-1) with Hoagland nutrient solution. Shoot dry weight reduced in both ferns at 160 mg As L-1 with higher decline in A. pinnata than A. prolifera. Fronds accumulated considerably higher As than roots but, compared to A. pinnata, A. prolifera transferred greater amount of As aboveground. Proper coordination among antioxidant defense facilitated high As accumulation in both ferns, but they differed in mechanistic responses. Reduced activities of ascorbate (AsA)-glutathione (GSH) cycle enzymes and increased level of γ-glutamyl transpeptidases (γ-GT) resulted in significant decline in GSH and AsA redox in A. pinnata at 160 mg As L-1. Contrastingly, powered by increased antioxidant defense capacity and reduced level of γ-GT, A. prolifera prevented As-induced oxidative damage. As triggered oxidative damage in A. pinnata through membrane lipid peroxidation and electrolyte leakage at 160 mg As L-1. This consequently inhibited plant growth and As accumulation potential of the aquatic fern.
Key words: Ampeloptens prolifera, Azolla pinnata, Aresenate, antioxidant, oxidative damage.
REFERENCES
- Beyer, W.F. and Fridovich, I. 1987. Assaying for superoxide dismutase activity: some large consequences of minor changes in condition. Anal. Biochem. 161: 559-566.
- Bradford, M.M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein–dye binding. Anal. Biochem. 72: 248-254.
- [3].Cao, X., Ma, L., Shiralipour, A. and Harris, W. 2014. Biomass reduction and arsenic transformation during composting of arsenic-rich hyperaccumulator Pteris vittata L. Environ. Sci. Pollut. Res. 17: 586-594.
- Carlberg, I. and Mannervik, B. 1985. Glutathione reductase. In: Methods in enzymology, Alton M, editor. Academic Press, San Diego, pp. 484-490
- Cedergreen, N. 2008. Is the growth stimulation by low doses of glyphosate sustained over time? Environ. Pollut. 156: 1099-1104.
- Dionisio-Sese, M. and Tobita, S. 1998. Antioxidant responses of rice seedlings to salinity stress. Plant Sci. 135: 1-9.
- Elstner, E.F. and Heupel, A. 1976. Inhibition of nitrate formation from hydroxyl ammonium chloride: a simple assay for superoxide dismutase. Anal. Biochem. 70: 616-620.
- Finnegan, P.M. and Chen, W. 2012. Arsenic toxicity: the effects on plant metabolism. Front. Physio. 3: 182.
- Flora, S.J.S., Bhadauria. S., Kannan. G.M. and Singh, N. 2007. Arsenic induced oxidative stress and the role of antioxidant supplementation during chelation: A review. J. Environ. Biol. 28: 333-347.
- Girdhar, M., Sharma. N.R., Rehman. H., Kumar. A. and Mohan, A. 2014. Comparative assessment for hyperaccumulatory and phytoremediation capability of three wild weeds. 3 Biotech. 4: 579-589.
- Griffith, O.W. 1980. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 106: 207-212.
- Guimaraes, F.P., Aguiar. R., Oliveira. J.A., Silva. J.A.A. and Karam, D. 2012. Potential of macrophyte for removing arsenic from aqueous solution. Planta Daninha, Viçosa-MG. 30: 683-696.
- Hodges, D.M., Delong, J.M., Forney, C.F. and Prange, R.K. 1999. Improving the thiobarbituric acid-reactive substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta. 207: 604–611.
- Howden, R., Goldsbrough, P.B., Andersen, C.R. and Cobbett, C. S. 1995. Cadmium sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol. 107: 1059-1066.
- Kertulis-Tartar, G., Ma, L.Q., Tu, C. and Chirenje, T. 2006. Phytoremediation of an arsenic-contaminated site using Pteris vittata L.: a two-year study. Int. J. Phytoremediation. 8: 311-322.
- Kertulis-Tartar, G.M., Rathinasabapathi, B. and Ma, L.Q. 2009. Characterization of glutathione reductase and catalase in the fronds of two Pteris ferns upon arsenic exposure. Plant Physiol. Biochem. 47: 960-965.
- Law, M.Y., Charles, S.A. and Halliwell, B. 1983. Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplast. The effect of hydrogen peroxide and paraquat. Biochem J. 10: 899-903.
- Li, Z-S., Zhen, R-G. and Rea, P.A. 1995. 1-chloro-2,4-dinitrobenzeneelicited increase in vacuolar glutathione-S-conjugate transport activity. Plant Physiol. 109: 177-185.
- Lichthenthaler, H.K. 1987. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Methods in enzymology, S. P. Colowick and N. O. Kaplan NO (Eds). Academic Press, San Diego, pp. 350-382
- Ma, L.Q., Komar, K.M., Tu, C., Zhang, W, Cai, Y. and Kennelley E.D. 2001. A fern that hyperaccumulates arsenic. Nature. 409: 579.
- Meharg, A.A. 2003. Variation in arsenic accumulation–hyperaccumulation in ferns and their allies. New Phytol. 157: 25-31.
- Mishra, S., Srivastava, S., Tripathi, R.D. and Trivedi, P.K. 2008. Thiol metabolism and antioxidant systems complement each other during arsenate detoxification in Ceratophyllum demersum L. Aquat. Toxicol. 86: 205-215.
- Moradi, S., Yosefi, R. and Ghaderi, O. 2013. Bioconcentration factor and relative growth rate of Azolla (Azolla caroliniana) in arsenic and salinity stress conditions. Int. J. Agron. Plant Prod. 4:2617-2623.
- Mukherjee, S. and Kumar, S. 2005. Adsorptive uptake of arsenic (V) from water by aquatic fern Salvinia natans. J. Water Supply: Res T- AQUA. 54: 47-53.
- Lingaiah, Estari Mamidala and P. Nagaraja Rao (2016). Modulatory effect of Cassia
auriculata plant extraction on glucose metabolism in alloxan induced diabetic Wistar rats.
The Ame J Sci & Med Res, 1(2); 212-220. doi:10.17812/ajsmr1213. - Nakano, Y. and Asada, K. 1981. Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 22: 867-880.
- Noctor, G., Mhamdi, A, Chaouch, S. et al. 2012. Glutathione in plants: an integrated overview. Plant Cell Environ. 35:454-484.
- Outridge, P.M. and Hutchinson, T.C. 1991. Induction of cadmium tolerance by acclimation transferred between ramets of clonal fern Salvinia minima Baker. New Phytol. 117: 597-605.
- Orlowski, M. and Meister, A. 1973. γ-Glutamyl cyclotransferase distribution, isozymic forms, and specificity. J. Biol. Chem. 248: 2836-2844.
- Pabby, A., Ahluwalia, A.S. and Dua, S. 2002. Temperature stress induced changes in growth and biochemical constituents of Azolla microphylla and Azolla pinnata. Indian J. Plant Physi. 7: 140-145.
- Pabby, A., Prasanna, R. and Singh, P.K. 2004. Biological significance of Azolla and its utilization in agriculture. Proc. Ind. Natl. Sci. Acad. B. 70: 301-335.
- [32].Patra, B. and Bera, S. 2007. Herbivore damage to ferns caused by a Chrysomelid beetle from lower Gangetic plains of West Bengal, India. Amer. Fern. J. 97:19-29.
- Połe´c-Pawlak, K., Ruzik, R., Abramski, K., Ciurzy´nska, M. and Gawro´nska, H. 2005. Cadmium speciation in Arabidopsis thaliana as a strategy to study metal accumulation system in plants. Anal. Chim. Acta. 540: 61-70.
- Prasad, S.M. and Singh, A. 2011. Metabolic responses of Azolla pinnata to cadmium stress: photosynthesis, antioxidative system and phytoremediation. Chem. Ecol. 27: 543-555.
- Rai, P.K. 2010. Microcosom investigation of phytoremediation of Cr using Azolla pinnata. Int. J. Phytoremediation. 12: 96-104.
- [36].Sánchez-Viveros, G., Ferrera-Cerrato, R. and Alarcón, A. 2011. Short-term effects of arsenate-induced toxicity on growth, chlorophyll and carotenoid contents, and total content of phenolic compounds of Azolla filiculoides. Water Air Soil Pollut. 217: 455-462.
- [37].Sánchez-Viveros, G., Ruvalcaba-Sil, J.L., Ferrera-Cerrato Alarcón, R.A. and Xoconostle-Cázares, B. 2015. Changes in elemental content in fronds of Azolla filiculoides due to arsenic accumulation. Plant Biosystems. in press. doi:10.1080/11263504.2015.1057257
- Sarkar, A. and Jana, S. 1986. Heavy metal pollutant tolerance of Azolla pinnata. Water Air Soil pollut. 27: 15-18.
- Seelig, G.F. and Meister, A. 1984. γ-Glutamylcysteine synthetase. J. Biol. Chem. 259: 3534-3538.
- Singh, A., Kumar, C.S. and Agarwal, A. 2013. Effect of lead and cadmium on aquatic plant Hydrilla verticillata. J. Environ. Biol. 34: 1027-1031.
- Singh, N. and Ma, L.Q. 2006. Arsenic speciation and arsenic and phosphate distribution in arsenic hyperaccumulator Pteris vittata L. and non-hyperaccumulator Pteris ensiformis L. Environ. Pollut. 141: 238–246.
- Singh, N., Ma, L.Q., Srivastava, M. and Rathinasabapathi, B. 2006. Metabolic adaptations to arsenic-induced oxidative stress in Pteris vittata L. and Pteris ensiformis L. Plant Sci. 170: 274–282.
- Singh, N., Raj, A., Khare, P.B., Tripathi, R.D. and Jamil, S. 2010. Arsenic accumulation pattern in 12 Indian ferns and assessing the potential of Adiantum capillus-veneris, in comparison to Pteris vittata, as arsenic hyperaccumulator. Bioresource Technol. 101: 8960–8968.
- Sood, A., Pabbi, S. and Uniyal, P.L. 2011. Effect of paraquat on lipid peroxidation and antioxidant enzymes in aquatic fern Azolla microphylla Kual. Russ. J. Plant Physiol. 58: 667-673.
- Sood, A., Uniyal, P.L., Prasanna, R. and Ahluwalia, A.S. 2014. Phytoremediation potential of aquatic macrophyte, Azolla. AMBIO. 41:122-137.
- Srivastava, M., Ma, L.Q., Singh, N. and Singh, S. 2005. Antioxidant responses of hyperaccumulator and sensitive fern species to arsenic. J. Exp. Bot. 56: 1335-1342.
- Srivastava, M., Santos, J., Srivastava, P. and Ma, L.Q. 2010. Comparison of arsenic accumulation in 18 fern species and four Pteris vittata. Bioresource Technol. 101: 2691–2699.
- Srivastava, S., Mishra, S., Tripathi, R.D., Dwivedi, S., Trivedi, P.K. and Tandon, P.K. 2007. Phytochelatins and antioxidant systems respond differentially during arsenite and arsenate stress in Hydrilla verticillata (L.f.) Royle. Environ. Sci. Technol. 41: 2930-2936.
- Sufian, J., Golchin, A., Avanes, A. and Moradi, S. 2013. Potentials of Azolla (Azolla caroliniana) for uptake of Arsenic from contaminated waters with different levels of salinity. Intl. J. Agri. Crop Sci. 6: 778-783.
- Swapna Gurrapu and Estari Mamidala. In Vitro HIV-1 Reverse Transcriptase Inhibition By
Alkaloids Isolated From Leaves Of Eclipta Alba.. International Research Journal of Pharmacy.
2018, 9 (1). 66-70. DOI: 10.7897/2230-8407.09110. - Talukdar, D. 2012. Ascorbate deficient semi-dwarf asfL1 mutant of Lathyrus sativus exhibits alterations in antioxidant defense. Biol. Plant. 56: 675-682.
- Talukdar, D. 2013a. Arsenic-induced oxidative stress in the common bean legume, Phaseolus vulgaris L. seedlings and its amelioration by exogenous nitric oxide. Physiol. Mol. Biol. Plants. 19: 69-79.
- Talukdar, D. 2013b. Plant growth and leaf antioxidant metabolism of four elite grass pea (Lathyrus sativus) genotypes, differing in arsenic tolerance. Agric. Res. 2: 330-339.
- Talukdar, D. 2013c. Floristic compositions and diversity of weed taxa in lentil (Lens culinnaris Medik.) fields. Bull. Env. Pharmacol. Life Sci. 2: 33-39.
- Talukdar, D. 2014. A common bean (Phaseolus vulgaris) mutant with constitutively low cysteine desulfhydrase activity exhibits growth inhibition but uniquely shows tolerance to arsenate stress. Environ. Exp. Biol. 12: 73-81.
- Talukdar, D. 2015. Functional interplay between glutathione and hydrogen sulfide in regulation of thiol cascade during arsenate tolerance of common bean (Phaseolus vulgaris L.) genotypes. 3 Biotech. 5: 819-829.
- Talukdar, D. and Talukdar, T. 2014. Coordinated response of sulfate transport, cysteine biosynthesis and glutathione-mediated antioxidant defense in lentil (Lens culinaris Medik.) genotypes exposed to arsenic. Protoplasma. 251:839–855.
- Talukdar, T. and Talukdar, D. 2015. Heavy metal accumulation as phytoremediation potential of aquatic macrophyte, Monochoria vaginalis (Burm. F.) K. Presl ex. kunth. Int. J. Appl. Sci. Biotechnol. 3: 9-15.
- Tripathi, P., Tripathi, R.D., Singh, R.P., Dwivedi, S., Chakrabarty, D., Trivedi, P.K. and Adhikari, B. 2013. Arsenite tolerance in rice (Oryza sativaL.) involves coordinated role of metabolic pathways of thiols and amino acids. Environ. Sci. Pollut. Res. 20: 884-896.
- Tu, C. and Ma, L.Q. 2005. Effects of arsenic on concentration and distribution of nutrients in the fronds of the arsenic hyperaccumulator Pteris vittata L. Environ. Pollut. 135: 333-340.
- Veljovic-Jovanovic, S.D., Pignocchi, C., Noctor, G. and Foyer, C.H. 2001. Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiol. 127: 426-435.
- Wang, C.Q., Chen, M. and Wang, B.S. 2007. Betacyanin accumulation in the leaves of C3 halophyte Suaeda salsa L. is induced by watering roots with H2O2. Plant Sci. 172:1-7.
- Wang, H.B., Wong, M.H., Lan, C.Y., Baker, A.J.M., Qin, Y.R., Shu, W.S., Chen, G.Z. and Ye, Z.H. 2007. Uptake and accumulation of arsenic by 11 Pteris taxa from southern China. Environ. Pollut. 145: 225-233.
- Zhang, X., Lin, A.J., Zhao, F.J., Xu,, G.Z., Duan, G.L. and Zhu, Y.G. 2008. Arsenic accumulation by the aquatic fern Azolla: Comparison of arsenate uptake, speciation and efflux by Azolla caroliniana and Azolla filiculoides. Environ. Pollut. 156: 1149–1155.
- Zhao, F.J., Ma, J.F., Meharg, A.A. and McGrath, S.P. 2009. Arsenic uptake and metabolism in plants. New Phytol. 181: 777–794.