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Response of growth, antioxidant enzymes and root exudates production towards As stress in Pteris vittata and in Astragalus sinicus colonized by arbuscular mycorrhizal fungi

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Abstract

The modern agricultural practices have led to improve the contaminated soils with a variety of heavy metals that have become a major environmental concern. The use of arbuscular mycorrihizal fungi (AMF) is considered a potential tool for the sustainable agriculture especially in contaminated sites. Moreover, recently, the use of AMF has become a fascinating and multidisciplinary subject for the scientists dealing with plant protection. The present study was carried out to evaluate the interaction among arsenic (As) species, AMF, and two plant species: Pteris vittata and Astragalus sinicus, differing in their metal tolerance. Results about A. sinicus revealed that the biomass was affected as As (III and V) accumulated in the roots of A. sinicus, and in rachis and pinnae of P. vittata. The inoculation of AMF markedly increased the biomass yield of the both plants when exposed to As species. The exposure to the As species resulted variation and non-significant results about antioxidant enzymes and non-enzymes when grown in As stress with and without AMF. The inoculation of AMF under As species improved the organic acids concentrations in both plant species. Overall, the concentration of oxalate acid was more than formic and malic acids; however, AMF inoculation improved more organic acids in A. sinicus. P. vittata exhibited more activities of antioxidant enzymes and non-enzymes under As stress with and without AMF than A. sinicus, and hence had a more efficient defense mechanism.

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References

  • Abd_Allah EF, Hashem A, Alqarawi AA, Alwathnani HA (2015) Alleviation of adverse impact of cadmium stress in sunflower (Helianthus annuus L.) by arbuscular mycorrhizal fungi. Pak J Bot 47(2):785–795

    CAS  Google Scholar 

  • Aebi HE, Bergmeyer HO (1983) Catalase, methods enzymology. Academic, New York, p 2

    Google Scholar 

  • Ahmad A, Hadi F, Ali N (2015) Effective phytoextraction of cadmium (Cd) with increasing concentration of total phenolics and free proline in Cannabis sativa (L) plant under various treatments of fertilizers, plant growth regulators and sodium salt. Int J Phytor 17:56–65

    Article  CAS  Google Scholar 

  • Aibibu N, Liu Y, Zeng G, Wang X, Chen B, Song H, Xu L (2010) Cadmium accumulation in vetiveria zizanioides and its effects on growth, physiological and biochemical parameters. Bioresour Technol 101:6297–6303

    Article  CAS  Google Scholar 

  • Alqarawi AA, Abd_Allah EF, Hashem A (2014) Alleviation of salt-induced adverse impact via mycorrhizal fungi in Ephedra aphylla Forssk. J Plant Interact 9(1):802–810

    Article  CAS  Google Scholar 

  • Anderson ME (1985) Determination of glutathione and glutathione disulphide in biological samples. Methods Enzymol 113:548–555

    Article  CAS  Google Scholar 

  • Anjum NA, Umar S, Ahmad A, Iqbal M (2008) Responses of components of antioxidant system in moongbean genotypes to cadmium stress. Commun Soil Sci Plant Anal 39:2469–2483

    Article  CAS  Google Scholar 

  • Asada K (1992) Ascorbate peroxidase–a hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85(2):235–241

    Article  CAS  Google Scholar 

  • Auge R (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Barrameda-Medina Y, Montesinos-Pereira D, Romero L, Ruiz JM, Blasco B (2014) Comparative study of the toxic effect of Zn in Lactuca sativa and Brassica oleracea plants: I. Growth, distribution, and accumulation of Zn, and metabolism of carboxylates. Environ Exp Bot 107:98–104

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  Google Scholar 

  • Cao XD, Ma LQ, Tu C (2004) Antioxidative responses to arsenic in the arsenic hyperaccumulator Chinese brake fern (Pteris vittata L.). Environ Pollut 128(3):317–325

    Article  CAS  Google Scholar 

  • Castillo FI, Penel I, Greppin H (1984) Peroxidase release induced by ozone in Sedum album leaves. Plant Physiol 74:846–851

    Article  CAS  Google Scholar 

  • Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34(1):33–41

    Article  Google Scholar 

  • Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23:867–902

    Article  CAS  Google Scholar 

  • Érico MMF, Ana PFS, Julio CPM, Edson IM, Juliana SFP, José NGP, Valderi LD (2009) Determination of Cd and Pb in medicinal plants using solid sampling flame atomic absorption spectrometry. Intern J Environ Anal Chem 89:129–140

    Article  CAS  Google Scholar 

  • Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci 86:528–534

    CAS  Google Scholar 

  • Goldberg S (2002) Competitive adsorption of arsenate and arsenite on oxides and clay minerals. Soil Sci Soc Am J 66(2):413–421

    Article  CAS  Google Scholar 

  • Gopi R, Jaleel CA, Sairam R, Lakshamanam GMA, Gomathinayagam M, Paneerselvam R (2007) Differential effects of hexaconazole and paclobutrazol on biomass, electrolyte leakage, lipid peroxidation and antioxidant potential of Daucus carota L. Colloids Surf B Biointerfaces 60(180):186

    Google Scholar 

  • Gratao PL, Gomes-Junior RA, Delite FS, Lea PJ, Azevedo RA (2006) Antioxidant stress responses of plants to cadmium. In: Khan NA, Samiullah (eds) Cadmium toxicity and tolerance in plants. Narosa Publishers, New Delhi, India, pp 1–34

    Google Scholar 

  • Guo T, Zhang G, Zhou M, Wu F, Chen J (2004) Effects of aluminum and cadmium toxicity on growth and antioxidant enzyme activities of two barley genotypes with different Al resistance. Plant Soil 258(1):241–248

    Article  CAS  Google Scholar 

  • Gupta M, Sharma P, Sarin NB, Sinha AK (2009) Differential response of arsenic stress in two varieties of Brassica juncea L. Chemosphere 74(9):1201–1208

    Article  CAS  Google Scholar 

  • Hashem A, Abd_Allah EF, Alqarawi AA, El-Didamony G, Alwhibi Mona S, Egamberdieva D, Ahmad P (2014) Alleviation of adverse impact of salinity on faba bean (Vicia faba L.) by arbuscular mycorrhizal fungi. Pak J Bot 46(6):2003–2013

    Google Scholar 

  • Hashem A, Abd_Allah EF, Alqarawi AA, Asma A, Al Huqail D, Egamberdieva SW (2016) Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi J Biol Sci 23(2):272–281

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts I. Kinetics and stoichiometery of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364

    Article  CAS  Google Scholar 

  • Kong F, Hu W, Chao S, Sang W, Wang L (1999) Physiological responses of the lichen Xanthoparmelia mexicana to oxidative stress of SO2. Environ Exp Bot 42(3):201–209

    Article  CAS  Google Scholar 

  • Koricheva J, Roy S, Vranjic JA, Haukioja E, Hughes PR, Hänninen O (1997) Antioxidant responses to simulated acid rain and heavy metal deposition in birch seedlings. Environ Pollut 95(2):249–258

    Article  CAS  Google Scholar 

  • Li CC, Kao CH (2000) Effect of NaCl stress on H2O2 metabolism in rice leaves. Plant Growth Regul 30(2):151–155

    Article  Google Scholar 

  • Liu L, Sun H, Chen J, Zhang Y, Li D, Li C (2014) Effects of cadmium (Cd) on seedling growth traits and photosynthesis parameters in cotton. P Omic J 7(4):284–290

    CAS  Google Scholar 

  • Mascher R, Lippmann B, Holzinger S, Bergmann H (2002) Arsenate toxicity: effects on oxidative stress response molecules and enzymes in red clover plants. Plant Sci 163(5):961–969

    Article  CAS  Google Scholar 

  • Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178

    CAS  Google Scholar 

  • Pätsikkä E, Kairavuo M, Šeršen F, Aro EM, Tyystjärvi E (2002) Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiol 129(3):1359–1367

    Article  CAS  Google Scholar 

  • Pawlowska TE, Charvat I (2004) Heavy-metal stress and developmental patterns of arbuscular mycorrhizal fungi. Appl Environ Microbiol 70:6643–6649

    Article  CAS  Google Scholar 

  • Repetto O, Massa N, Gianinazzi-Pearson V, Dumas-Gaudot E, Berta G (2007) Cadmium effects on populations of root nuclei in two pea genotypes inoculated or not with the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza 17:111–120

    Article  CAS  Google Scholar 

  • Singh R, Singh S, Parihar P, Singh VP, Prasad SM (2015) Arsenic contamination, consequences and remediation techniques: a review. Ecotoxicol Environ Saf 112:247–270

    Article  CAS  Google Scholar 

  • Srivastava S, Tripathi RD, Dwivedi UN (2004) Synthesis of phytochelatins and modulation of antioxidants in response to cadmium stress in Cuscuta reflexa-an angiospermic parasite. J Plant Physiol 161:665–674

    Article  CAS  Google Scholar 

  • Tiryakioglu M, Eker S, Ozkutlu F, Husted S, Cakmak I (2006) Antioxidant defense system and cadmium uptake in barley genotypes differing in cadmium tolerance. J Trace Ele Med Biol 20:181–189

    Article  CAS  Google Scholar 

  • Trotta A, Falaschi P, Cornara L, Minganti V, Fusconi A, Drava G, Berta G (2006) Arbuscular mycorrhizae increase the arsenic translocation factor in the As hyperaccumulating fern Pteris vittata L. Chemosphere 65:74e81

    Article  CAS  Google Scholar 

  • Tu S, Ma LQ (2003) Interactive effects of pH, arsenic and phosphorus on uptake of As and P and growth of the arsenic hyperaccumulator Pteris vittata L. under hydroponic conditions. Environ Exp Bot 50:243–251

    Article  CAS  Google Scholar 

  • Tu S, Ma L, Luongo T (2004) Root exudates and arsenic accumulation in arsenic hyperaccumulating Pteris vittata and non-hyperaccumulating Nephrolepis exaltata. Plant Soil 258(1):9–19

    Article  CAS  Google Scholar 

  • Wang P, Zhou R (2006) Determination of organic acids exuded from plant roots by high performance liquid chromatography. China J Chromatogr 24:239–242

    Article  CAS  Google Scholar 

  • Wu F, Ye Z, Wong M (2009) Intraspecific differences of arbuscular mycorrhizal fungi in their impacts on arsenic accumulation by Pteris vittata L. Chemosphere 76(9):1258–1264

    Article  CAS  Google Scholar 

  • Wu QS, Zou YN, Abd_Allah EF (2014) Mycorrhizal association and ROS in plants. In: P. Ahmad (Ed): Oxidative Damage to Plants. 2014. doi: https://doi.org/10.1016/B978-0-12-799963-0.00015-0. Elsevier Inc.

  • Xie QE, Yan XL, Liao XY, Li X (2009) The arsenic hyperaccumulator fern Pteris vittata L. Environ Sci Technol 43(22):8488–8495

    Article  CAS  Google Scholar 

  • Xie YJ, Xu S, Han B, Wu MZ, Yuan XX, Han Y, Gu Q, Xu DK, Yang Q, Shen WB (2011) Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J 66(2):280–292

    Article  CAS  Google Scholar 

  • Xiong SL, Song JY, Tu SX, Jin O, Yu FJ, Du W, Chen YF, Tan QL, Yang JC (2012) Arsenic tolerance of oilseed mustard (Brassica juncea) genotypes. Chinese J Oil Crop Sci 3:009

    Google Scholar 

  • Zhang HH, Tang M, Chen H, Zheng CL, Niu ZC (2010) Effect of inoculation with AM fungi on lead uptake, translocation and stress alleviation of Zea mays L. seedlings planting in soil with increasing lead concentrations. Eur J Soil Biol 46:306–311

    Article  Google Scholar 

  • Zhang RQ, Zhu HH, Zhao HQ, Yao Q (2013) Arbuscular mycorrhizal fungal inoculation increases phenolic synthesis in clover roots via hydrogen peroxide, salicylic acid and nitric oxide. signaling pathways. J Plant Physiol 170:74–79

    Article  CAS  Google Scholar 

  • Zheng Y, Ayotte JD (2015) At the crossroads: hazard assessment and reduction of health risks from arsenic in private well waters of the northeastern United States and Atlantic Canada. Sci Total Environ 505:1237–1247

    Article  CAS  Google Scholar 

Download references

Funding

This research was supported in part by the Guangxi Major Special Project of Science and Technique (GuikeAA17202026-3), Hubei Special Project for Technique Innovation (2017ABA154), and Special Fund for Agro-scientific Research in the Public Interest (201303106).

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Authors and Affiliations

  1. Institute of Agriculture Resources and Regional Planning, Chinese Academy of Agriculture Sciences, Beijing, 100081, China

    Liu Yizhu

  2. Soil and Environmental Biotechnology Division, National Institute for Biotechnology and Genetic Engineering (NIBGE), Faisalabad, Pakistan

    Muhammad Imtiaz & Fathia Mubeen

  3. Department of Environmental Sciences, Shaheed Benazir Bhutto University, Sheringal, Dir (U), 18000, Pakistan

    Allah Ditta

  4. Cholistan Institute of Desert Studies, The Islamia University of Bahawalpur, Bahawalpur, 63100, Pakistan

    Muhammad Shahid Rizwan

  5. Department of Soil Science, Bahauddin Zakariya University, Multan, Pakistan

    Muhammad Ashraf

  6. Guangdong Provincial Key Laboratory for Radionuclides Pollution Control and Resources, School of Environmental Science and Engineering, Guangzhou University, Guangzhou, 510006, China

    Sajid Mehmood

  7. University of Agriculture Faisalabad, Faisalabad, Sub-Campus Depalpur, Okara, Pakistan

    Omar Aziz

  8. Department of Biotechnology, COMSATS University Islamabad, Abbottabad campus, Abbottabad, Pakistan

    Muhammad Ali

  9. Institute of Pure and Applied Biology, Bahauddin Zakariya University, Multan, Pakistan

    Nosheen Noor Elahi

  10. Department of Horticulture, The University of Poonch Rawalakot, Rawalakot, Azad Kashmir, Pakistan

    Raina Ijaz

  11. Suzhou Leju Holdings Limited, Suzhou, Jiangsu, China

    Sha Lele

  12. Wuhan Environmental Protection Sciences Research Institute, Wuhan, China

    Cao Shuang

  13. College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, China

    Shuxin Tu

  14. Microelement Research Center, Huazhong Agricultural University, Wuhan, 430070, China

    Shuxin Tu

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  1. Liu Yizhu
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Yizhu, L., Imtiaz, M., Ditta, A. et al. Response of growth, antioxidant enzymes and root exudates production towards As stress in Pteris vittata and in Astragalus sinicus colonized by arbuscular mycorrhizal fungi. Environ Sci Pollut Res 27, 2340–2352 (2020). https://doi.org/10.1007/s11356-019-06785-5

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  • DOI: https://doi.org/10.1007/s11356-019-06785-5

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