The Cadmium Toxicity in Helianthus annuus can be Modulated by Endosymbiotic Fungus (Piriformospora indica)

Document Type : Research Article

Authors

1 Department of Biology, Faculty of Science, University of Maragheh, Maragheh, Iran

2 Department of Agronomy, Faculty of Agriculture, University of Maragheh, Maragheh, Iran University of Maragheh, Madar Square, Golshahr, Maragheh, Iran

Abstract

Cadmium (Cd), as a widespread metal pollutant, readily accumulates in the food chain due to its easy absorption and high mobility. The endophytic fungi are cosmopolitan microorganisms that occur widely in association with plants in a heavy metal stress environment. A current pot experiment was conducted to evaluate the influence of Piriformospora indica, as a root endosymbiotic fungus, on the biomass and biochemical responses of sunflower cv. Zaria under excessive Cd concentrations (0, 40, 80 and 120 mg Cd/kg) in the soil, in a 2 × 4 factorial randomized block design in five replicates. In response to increasing Cd levels in soil, root colonization, growth parameters, and total chlorophyll and carotenoids contents were significantly reduced (P < 0.05), whereas root and leaf Cd accumulation, malondialdehyde (MDA) amount and the antioxidant enzymes activities of catalase (CAT), guaiacol peroxidase (POD), ascorbate peroxidase (APX) and superoxide dismutase (SOD) were increased (P < 0.05). Under different levels of Cd in soil, presence of P. indica (in inoculated sunflowers) had a significant increase (P < 0.05) on growth rate, photosynthesis pigments content, root Cd accumulation, and activities of CAT, POD, APX and SOD in compare to absence of P. indica (in non-inoculated ones). Also, P. indica-inoculated plants showed a reduced MDA concentration and leaf Cd accumulation than un-inoculated sunflowers. The results indicated that P. indica, as an appropriate fungal association, can improve tolerance of sunflower to Cd toxicity through increased levels of photosynthesis pigments and antioxidants, and reduced Cd accumulation and MDA content of the leaf. Therefore, this root endophyte can be modulated cadmium toxicity in Helianthus annuus under excessive cadmium in soil, and recommended as a complement crop-growing strategy in the fields under Cd-contaminated soils, for other studies.
 

Keywords

References

Aebi H. 1984. Catalase in vitro. Methods Enzymol 105: 121-126.
Aishwarya S, Venkateswarlu N, Chandramouli K, Vijaya T. 2014. Role of endophytic fungi in the restoration of heavy metal contaminated soils. Indo Am j Pharm Sci 4: 5427-5436.
Arnon A. 1967. Method of extraction of chlorophyll in the plants. Agron J 23: 112-121.
Awotoye OO, Adewole MB, Salami AO, Ohiembor MO. 2009. Arbuscular mycorrhiza contribution to the growth performance and heavy metal uptake of Helianthus annuus LINN in pot culture. Afr J Environ Sci Technol 3 (6): 157-63.
Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel KH, Schäfer P, Schwarczinger I, Zuccaro A, Skoczowski A. 2008. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180 (2): 501-510.
Bashri G, Prasad SM. 2015. Indole acetic acid modulates changes in growth, chlorophyll a fluorescence and antioxidant potential of Trigonella foenumgraecum L. grown under cadmium stress. Acta Physiol Plant 37: 49.
Benavides M, Gallego SM, Tomaro ML. 2005. Cadmium toxicity in plants. Braz J Plant Physiol 17 (1): 49-55.
Borišev M, Pajević S, Nikolić N, Krstić B, Župunski M, Kebert M, Pilipović A, Orlović S. 2012. Response of Salix alba L. to heavy metals and diesel fuel contamination. Afr J Biotechnol 11 (78): 14313-14319.
Bradford MM. 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.
Broadley MR, Willey NJ, Wilkins JC, Baker AJM, Mead A, White PJ. 2001. Phylogenetic variation in heavy metal accumulation in angiosperms. New Phytol 152 (1): 9-27.
Chance A, Maehly AC. 1955. Assay of catalases and peroxidase. Methods Enzymol 2: 764-775.
Chaoui A, Ferjani EE. 2005. Effects of cadmium and copper on antioxidant capacities, lignification and auxin degradation in leaves of pea (Pisum sativum L.) seedlings. C R Biol 328 (1): 23-31.
Cornu JY, Bakoto R, Bonnard O, Bussière S, Coriou C, Sirguey C, Sterckeman T, Thunot S, Visse MI, Nguyen C. 2016. Cadmium uptake and partitioning during the vegetative growth of sunflower exposed to low Cd2+ concentrations in hydroponics. Plant Soil 404: 263-275.
Del Rio D, Stewart AJ, Pellegrini N. 2005. A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 15 (4): 316-328.
Dhindsa RS, Matowe W. 1981. Drought tolerance in two mosses: correlated with enzymatic defense against lipid peroxidation. J Exp Bot 32(1): 79-91.
Faessler E, Robinson BH, Stauffer W, Gupta SK, Papritz A, Schulin R. 2010. Phytomanagement of metal-contaminated agricultural land using sunflower, maize and tobacco. ‎ Agric Ecosyst Environ 136 (1-2): 49-58.
Gill SS, Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48 (12): 909-930.
Göhre V, Paszkowski U. 2006. Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223 (6): 1115-1123.
Grant CA, Clarke JM, Duguid S, Chaney RL. 2008. Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 390 (2-3): 301-310.
Groppa MD, Ianuzzo MP, Rosales EP, Vazquez SC, Benavides MP. 2012. Cadmium modulates NADPH oxidase activity and expression in sunflower leaves. Biol Plant 56 (1): 167-171.
Hartley SE, Gange AC. 2009. Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54: 323-342.
Heath RL, Packer L. 1968. Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1): 189-198.
Hill TW, Käfer E. 2001. Improved protocols for Aspergillus minimal medium: trace element and minimal medium salt stock solutions. Fungal Genet Newsletter 48: 20-21.
Hui F., Liu J., Gao P., Lou B. 2015. Piriformospora indica confers cadmium tolerance in Nicotiana tabacum. J Environ Sci 37: 184-191.
John R, Ahmad P, Gadgil K, Sharma S. 2009. Cadmium and lead-induced changes in lipid peroxidation, antioxidative enzymes and metal accumulation in Brassica juncea L. at three different growth stages. Arch Agron Soil Sci 55(4): 395-405.
Khan AR, Ullah I, Waqas M, Park GS, Khan AL, Hong SJ, Ullah R, Jung BK, Park CE, Ur-Rehman S, Lee IJ, Shin JH. 2017. Host plant growth promotion and cadmium detoxification in Solanum nigrum, mediated by endophytic fungi. Ecotoxicol Environ Saf 136: 180-188.
Li FT, Qi JM, Zhang GY, Lin LH, Fang PP, Tao AF, Xu JT. 2013. Effect of Cadmium Stress on the Growth, Antioxidative Enzymes and Lipid Peroxidation in Two Kenaf (Hibiscus cannabinus L.) Plant Seedlings. J Integr Agric 12(4): 610-620
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 (1): 89-98.
Lin Y, Aarts MGM. 2012. The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69 (19): 3187-3206.
Maksymiec W, Krupa Z. 2006. The effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ Exp Bot 57 (1-2): 187-194.
Mohadjerani M, Naqinezhad A, Sharbaf MA. 2016. Platycladus orientalis Extracts with Antioxidant Activity from North of Iran. J Genet Resour 2(2): 60-66.
Nakano Y, Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22 (5): 867-880.
Oelmüller R, Sherameti I, Tripathi S, Varma A. 2009. Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 19 (1): 1-19.
Padash A, Shahabivand S, Behtash F, Aghaee A. 2016. A practicable method for zinc enrichment in lettuce leaves by the endophyte fungus Piriformospora indica under increasing zinc supply. Sci Hortic 213: 367-372.
Phillips JM, Hayman DS. 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55 (1): 158-161.
Qian H, Li J, Sun L, Chen W, Sheng GD, Liu W, Fu Z. 2009. Combined effect of copper and cadmium on Chlorella vulgaris growth and photosynthesis-related gene transcription. Aquat Toxicol 94 (1): 56-61.
Rascio N, Dalla Vecchia F, La Rocca N, Barbato R, Pagliano C, Raviolo M, Gonnelli C, Gabbrielli R. 2008. Metal accumulation and damage in rice (cv. Vialone nano) seedlings exposed to cadmium. Environ Exp Bot 62 (3): 267-278.
Saidi I, Chtourou Y, Djebali W. 2014. Selenium alleviates cadmium toxicity by preventing oxidative stress in sunflower (Helianthus annuus) seedlings. J Plant Physiol 171 (5): 85- 91.
Shahabivand S, Maivan HZ, Mahmoudi E, Soltani BM, Sharifi M, Aliloo AA. 2016. Antioxidant activity and gene expression associated with cadmium toxicity in wheat affected by mycorrhizal fungus. Žemdirbystė 103 (1): 53-60.
Shahabivand S, Parvaneh A, Aliloo AA. 2017. Root endophytic fungus Piriformospora indica affected growth, cadmium partitioning and chlorophyll fluorescence of sunflower under cadmium toxicity. Ecotoxicol Environ Saf 145: 496-502.
Shahabivand S, Zare-Maivan H, Goltapeh EM, Sharifi M, Aliloo AA. 2012. The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. Plant Physiol Biochem 60: 53-58.
Singh A, Prasad SM. 2014. Effect of agro-industrial waste amendment on Cd uptake in Amaranthus caudatus grown under contaminated soil: an oxidative biomarker response. Ecotoxicol Environ Saf 100: 105-113.
Sirrenberg ACG, Stephanie G, Czempinski N, Karlovsky ARP, Santos P, Katharina IF. 2007. Piriformospora indica affects plant growth by auxin production. Physiol Plant 131 (4): 581-589.
Sun C, Johnson J, Cai DG, Sherameti I, Oelmüller R, Lou BG. 2010. Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J Plant Physiol 167(12): 1009-1017.
Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. 2007. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39 (1): 44-84.
Varma A, Singh A, Sudha M, Sahay NS, Sharma J, Roy A, Kumari M, Rana D, Thakran S, Deka D, Bharti K, Hurek T, Blechert O, Rexer KH, Kost G, Hahn A, Maier W, Walter M, Strack D, Kranner I. 2001. Piriformospora indica: a cultivable mycorrhiza-like endosymbiotic fungus. In: Hock B, (Ed.). The Mycota IX. Springer-Verlag, Berlin, pp. 125-150.
Yu W-C, Lee J-T, Tsai B-H. 2011. Effects on Sunflower Growth Induced by Adding Different Soil Amendments to Cadmium-Contaminated Soil, in: Hu J, (Ed.). Advances in Biomedical Engineering, pp 74-79.
Zhao FJ, Mc Grath SP, Crosland AR. 1994. Comparison of three wet digestion methods for the determination of plant sulphur by inductively coupled plasma atomic emission spectroscopy (ICP AES). Commun Soil Sci Plant Anal 25 (3-4): 407-418.
Zoffoli HJ, do Amaral-Sobrinho NM, Zonta E, Luisi MV, Marcon G, Tolon Becerra A. 2013. Inputs of heavy metals due to agrochemical use in tobacco fields in Brazil’s southern region. Environ Monit Assess 185 (3): 2423-2437.
Journal of Genetic Resources
Volume 4, Issue 1
March 2018
Pages 44-55

Files

Share

How to cite

Statistics