Abstract
TiO2 nanoparticles (TiO2NPs) is one of the most widely used nanomaterials. Arbuscular mycorrhizal fungi (AMF) are an important and widely distributed group of soil microorganisms, which promote the absorption of nutrients by host plants and increase their tolerance to contaminants. However, the effects and mechanisms of AMF on plant TiO2NPs tolerance in wetland habitats are not clear. In this experiment, under the conditions of three soil moisture contents (drought 50%, normal 70% and flooding 100%) and four TiO2NPs concentrations (0, 100, 200 and 500 mg kg−1), the effects of Funneliformis mosseae on the growth, antioxidant enzyme activities, osmotic substances and the absorption and accumulation of Ti in the Phragmites australis (reed) seedlings were studied. The results showed that the inoculation of F. mosseae under three moisture content conditions significantly increased the plant nutrition and root activities of reeds. Compared with the non-inoculated control, inoculation with F. mosseae increased the activities of antioxidant enzymes, the contents of chlorophyll, proline, soluble protein, and free amino acids, and significantly reduced the contents of malondialdehyde (MDA) and reactive oxygen species (ROS) of leaves. The accumulating ability of inoculated reeds to Ti was significantly higher than that of non-inoculated controls (P < 0.05), and inoculation of F. mosseae changed the distribution of Ti in reeds, increased the accumulation of Ti in roots. It’s confirmed that inoculation of F. mosseae under three water conditions could improve the plant growth and nutrition, the activities of antioxidant enzymes, and enhance the reeds tolerance to TiO2NPs in this study.
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References
Asli S, Neumann PM (2009) Colloidal suspensions of clay or titanium dioxide nanoparticles can inhibit leaf growth and transpiration via physical effects on root water transport. Plant Cell Environ 32:577–584
Ban YH, Jiang YH, Li M, Zhang XL, Zhang SY, Wu Y, Xu ZY (2017) Homogenous stands of a wetland grass living in heavy metal polluted wetlands harbor diverse consortia of arbuscular mycorrzhial fungi. Chemosphere 181:699–709
Bello OA, Tawabini SB, Khalil BA, Boland RC, Saleh AT (2018) Phytoremediation of cadmium-, lead- and nickel-contaminated water by Phragmites australis in hydroponic systems. Ecol Eng 120:126–133
Birbaum K, Brogioli R, Schellenberg M, Martinoia E, Stark WJ, Cunther D, Limbach LK (2010) No evidence for cerium dioxide nanoparticle translocation in maize plants. Environ Sci Technol 44:8718–8723
Cao JL, Feng YZ, Lin XG (2017) Influence of arbuscular mycorrhizal fungi and iron oxide magnetic nanoparticles on maize growth and Fe-uptake. J Ecol Rural Environ 33:555–563
Chen YQ, Jiang L, Xu WH, Chi SL, Chen XG, Xie WW, Xiong SJ, Zhang JZ, Xiong ZT (2015) Effect of ryegrass and arbuscular mycorrhizal on Cd absorption by varieties of tomatoes and cadmium forms in soil. Environ Sci 36:4642–4650
Chen JF, Lu XJ, Zeng BJ, Gong YL, Liang WF, Deng CH, Ling WT, Li L (2017a) Advances in research on effects of arbuscular mycorrhizal fungi on accumulation of heavy metals in rhizosphere. Agric Res Appl 170:72–77
Chen X, Zheng ZX, Shi Q, Zhang FJ (2017b) Effect of AMF and plants on accumulation of Pb and Cd in soil. J Fungal Res 15:33–39
Concha-Guerrero SI, Brito EMS, Pinon-Castillo HA, Tarango-Rivero SH, Caretta CA, Luna-Velasco A, Duran R, Orrantia-Borunda E (2014) Effect of CuO nanoparticles over isolated bacterial strains form agricultural soil. J Nanomater 2014:1–13
Cooke JC, Butler RH, Madole G (1993) Some observations on the vertical distribution of vesicular arbuscular mycorrhizae in roots of salt marsh grasses growing in saturated soils. Mycologia 85:547–550
Du W, Sun Y, Ji R, Zhu J, Wu J, Guo H (2011) TiO2 and ZnO nanoparticles negatively affect wheat growth and soil enzyme activities in agricultural soil. J Environ Monit 13:822–828
Fester T (2013) Arbuscular mycorrhizal fungi in a wetland constructed for benzene-, methyl tert-butyl ether and ammonia-contaminated groundwater bioremediation. Microb Biotechnol 6:80–84
Gao JF (2006) Experimental guidance for plant physiology. Higher Education Press, Beijing
Ge L, Sun SB, Chen AQ, Kapulnik Y, Xu GH (2008) Tomato sugar transporter genes associated with mycorrhiza and phosphate. Plant Growth Regul 55:115–123
Ghosh M, Bandyopadhyay M, Mukherjee A (2010) Genotoxicity of titanium dioxide (TiO2) nanoparticles at two trophic levels, plant and human lymphocytes. Chemosphere 81:1253–1262
Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol Plant 138:226–237
Hu J, Wu S, Wu F, Leung HM, Leung X, Wong MH (2013) Arbuscular mycorrhizal fungi enhance both absorption and stabilization of Cd by alfred stonecrop (Sedum alfredii Hance) and perennial ryegrass (Lolium perenne L.) in a Cd-contaminated acidic soil. Chemosphere 93:1359–1365
Ipsilantis I, Sylvia D (2007) Abundance of fungi and bacteria in a nutrient impacted Florida wetland. Appl Soil Ecol 35:272–280
Keller AA, Lazareva A (2014) Predicted releases of engineered nanomaterials, from global to regional to local. Environ Sci Technol Lett 1:65–70
Kohout P, Sýkorová Z, Čtvrtlíková M, Rydlová J, Suda J, Vohník M, Sudová R (2012) Surprising spectra of root-associated fungi in submerged aquatic plants. FEMS Microbiol Ecol 80:216–235
Lan LZ, Zhao QF, Jin KX (2018) Effects of nano-TiO2 on growth and gene expression in Arabidopsis thaliana. J Nucl Agric Sci 32:0389–0398
Larue C, Laurette J, Herlin-boime N, Khodja H, Fayard B, Flank AM, Brisset F, Carriere M (2012) Accumulation, translocation and impact of TiO2 nanoparticles in wheat (Triticum aestivum spp.), influence of diameter and crystal phase. Sci Total Environ 431:197–208
Li HS (2000) Physiological and biochemical experimental principles and techniques. Higher Education Press, Beijing
Liu ZY, Yu SL, Liu GC, Du XJ, Wang XG (2013) Effect of different digesting methods on the detection of titanium dioxide nanoparticles concentration. Environ Chem 32:666–669
Liu CG, Dai Z, Cui MY, Lu WK, Sun HW (2018) Arbuscular mycorrhizal fungi alleviate boron toxicity in Puccinellia tenuiflora under the combined stresses of salt and drought. Environ Pollut 240:557–565
Lyu SH, Wei XY, Chen JJ, Wang C, Wang XM, Pan DM (2017) Titanium as a beneficial element for crop production. Front Plant Sci 8:597
Miller SP (2000) Arbuscular mycorrhizal coloization of semi-aquatic grasses along a wide hydrologic gradient. New Phytol 145:145–155
Ministry of Environmental Protection (2015) Report on the state of environment in China 2014. http://jcs.mep.gov.cn/hjzl/zkgb/2014zkgb/. Accessed 15 July 2015
Miransari M (2013) Plant, mycorrhizal fungi, and bacterial network. In: Hakeem KR, Rehman RU, Tahir I (eds) Plant signaling: understanding the molecular crosstalk. Springer, New Delhi, pp 315–325
Noori A, White JC, Newman LA (2017) Mycorrhizal fungi influence on silver uptake and membrane protein gene expression following silver nanoparticle exposure. J Nanopart Res 19:66
Nowack B, Ranville JF, Diamond S, Gallego-Urrea JA, Metcalfe C, Rose J, Horne N, Koelmans AA, Klaine SJ (2012) Potential scenarios for nanomaterial release and subsequent alteration in the environment. Environ Toxicol Chem 31:50–59
Pachapur VL, Larios AD, Cledón M, Brar SK, Verma M, Surampalli RY (2016) Behaviour and characterization of titanium dioxide and silver nanoparticles in soils. Sci Total Environ 563–564:933–943
Peat H, Fitter A (1993) The distribution of arbuscular mycorrhizas in the British flora. New Phytol 125:845–854
Phillips JM, Hayman DS (1970) Improved procedure for clearing and staining parastic and vesicular-arbuscular fungi for rapid assessment of infection. Trans Brit Mycol Soc 55:158–161
Pollastri S, Savvides A, Pesando M, Lumini E, Volpe MG, Ozudogru EA, Faccio A, De Cunzo F, Michelozzi M, Lambardi M, Fotopoulos V, Loreto F, Centritto M, Balestrini R (2018) Impact of two arbuscular mycorrhizal fungi on Arundo donax L. response to salt stress. Planta 247:573–585
Ruffini Castiglione M, Giorgetti L, Bellani L, Muccifora S, Bottega S, Spanò C (2016) Root responses to different types of TiO2 nanoparticles and bulk counterpart in plant model system Vicia faba L. Environ Exp Bot 130:11–21
Schreiber L (2011) Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci 15:546–553
Seeger EM, Baun A, Kanstner M, Trapp S (2009) Insignificant acute toxicity of TiO2 nanoparticles to willow trees. J Soil Sediment 9:46–53
Servin AD, Hernandez JA, Castillo-Michel H, Peralta-Videa J, Gardea-Torresdey J (2012) TiO2NPs can be taken up by roots and translocated to leaves in cucumber (Cucumis sativus) plants. Abstr Pap Am Chem Soc 244:193
Siani NG, Fallah S, Pokhrel LR, Rostamnejadi A (2017) Rostamnejadi. Natural amelioration of Zinc oxide nanoparticle toxicity in fenugreek (Trigonella foenum-gracum) by arbuscular mycorrhizal (Glomus intraradices) secretion of glomalin. Plant Physiol Biochem 112:227–238
Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic Press, Boca Raton
Song GL, Gao Y, Wu H (2012) Physiological effect of anatase TiO2 nanopatices on Lemma minor. Environ Toxicol Chem 31:2147–2152
Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A et al (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci 110:20117–22122
Tiwari M, Sharma NC, Fleischmann P, Burbage J, Venkatachalam P, Sahi SV (2017) Nanotitania exposure causes alterations in physiological, nutritional and stress responses in tomato (Solanum lycopersicum). Front Plant Sci 8:1–12
Twanabasu BR, Smith CM, Stevens KJ, Venables BJ, Sears WC (2013) Triclosan inhibits arbuscular mycorrhizal colonization in three wetland plants. Sci Total Environ 447:450–457
Vodnik D, Grcman H, Macek I, van Elteren JT, Kovacevic M (2008) The contribution of glomalin-related soil protein to Pb and Zn sequestration in polluted soil. Sci Total Environ 392:130–136
Vymazal J, Březinová T (2016) Accumulation of heavy metals in aboveground biomass of Phragmites australis in horizontal flow constructed wetlands for wastewater treatment: a review. Chem Eng J 290:232–242
Wang JY, Ao H, Zhang J (2003) Experimental techniques and principles of plant physiology and biochemistry. Northeast Forestry University Press, Harbin
Wang Y, Qiu Q, Yang Z, Hu Z, Tam NFY, Xin G (2010) Arbuscular mycorrhizal fungi in two mangroves in South China. Plant Soil 331:181–191
Wang SH, Zhang H, He QY (2011) Effects of copper stress on Medicago sativa seedlings leaf antioxidative system. Chin J Appl Ecol 22:2285–2290
Wang Z, Xie X, Zhao J, Liu X, Feng W, White JC, Xing B (2012) Xylem- and phloem-based transport of CuO nanoparticles in maize (Zea mays L.). Environ Sci Technol 46:4434–4441
Wang F, Liu X, Shi Z, Tong R, Adams CA, Shi X (2016) Arbuscular mycorrhizae alleviate negative effects of zinc oxide nanoparticle and zinc accumulation in maize plants: a soil microcosm experiment. Chemosphere 147:88–97
Wang FY, Adams CA, Shi ZY, Sun YH (2018) Combined effects of ZnO NPs and Cd on sweet sorghum as influenced by an arbuscular mycorrhizal fungus. Chemosphere 209:421–429
Wen SX, Wang YL (2017) Effect of nano titanium dioxide with different particle size on the seed germination and plant growth and physiology of Phragmites australis in hydroponic experiments. Asian J Ecotoxicol 12:71–80
Westerhoff P, Song G, Hristovski K, Kiser MA (2011) Occurrence and removal of titanium at full scale wastewater treatment plants: implications for TiO2 nanomaterials. J Environ Monitor 13(5):1195–1203
Wirsel SG (2004) Homogenous stands of a wetland grass harbour diverse consortia of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 48:129–138
Xie X, Weng B, Cai B, Dong Y, Yan C (2014) Effects of arbuscular mycorrhizal inoculation and phosphorus supply on the growth and nutrient uptake of Kandelia obovata (Sheue, Liu & Yong) seedlings in autoclaved soil. Appl Soil Ecol 75:162–171
Xu ZY, Ban YH, Jiang YH, Zhang XL, Liu XY (2016) Arbuscular mycorrhizal fungi in wetland habitats and their application in constructed wetland: a review. Pedosphere 26:592–617
Xu ZY, Wu Y, Jiang YH, Zhang XL, Li JL, Ban YH (2018) Arbuscular mycorrhizal fungi in two vertical-flow wetlands constructed for heavy metal-contaminated wastewater bioremediation. Environ Sci Pollut Res 25:12830–12840
Yang GW, Liu N, Yang X, Zhang YJ (2015) Relationship between arbuscular mycorrhizal fungi and individual plant and their effects on plant productivity and species diversity of plant community. Acta Prata Sin 24:188–203
Yin HG, Tang ZX, Tang KX, Cao WP (2017) The application of macrophytes in the water bioremediation fields: a review. Environ Sci Technol 30:67–70
Yuan J, Tan X, Ye S, Zhou N, Shi B (2013) The organic acids in root exudates of oil tea and its role in mobilization of sparingly soluble phosphate in red soil. J Chem Pharm Res 11:572–577
Ze YG, Liu C, Wang L, Hong MM, Hong FS (2011) The regulation of TiO2 nanoparticles on the expression of light-harvesting complex II and photosynthesis of chloroplasts of Arabidopsis thaliana. Biol Trace Elem Res 143:1131–1141
Zeng JH, Li YY, Ruan DS, Chao YQ, Qiu RL, Yang YH, Wang SZ (2017) Phytoremediation of heavy metal contaminated soils by plant growth-promoting rhizobacteria and arbuscular mycorrhizal fungi. Microbiol China 44:1214–1221
Zhang H, Peng C, Yang JJ, Shi JY (2013) Eco-toxicological effect of metal-based nanoparticles on plants. Chin J Appl Ecol 24:885–892
Zhang ZF, Zhang JC, Huang YQ (2014) Effects of arbuscular mycorrhizal fungi on the drought tolerance of Cyclobalanopsis glauca seedlings under greenhouse conditions. New For 45:545–556
Zhang X, Chen BD, Sun YQ, Wu SL, Li JL (2017) Advances in the study of interaction between arbuscular mycorrhizal fungi and arsenic. J Fungal Res 15:53–57
Zhang HH, Wang Y, Chen SN, Zhao ZF, Feng J, Zhang ZH, Lu KY, Jia JY (2018) Water bacterial and fungal community compositions associated with urban lakes, Xi’an, China. Int J Environ Res Public Health 15:469
Zhao X, Lin YE, Na XW, Li GC (2017) Influence of arbuscular mycorrhizal fungus on the osmotic adjustment substance and antioxidant system of Medicago sativa under salt-alkaline stress. J Agric Sci 33:782–787
Zu YQ, Lu X, Zhan FD, Hu WY, Li Y (2015) A review on roles and mechanisms of arbuscular mycorrhizal fungi in phytoremediation of heavy metals-polluted soils. Plant Physiol J 51:1538–1548
Acknowledgements
This research was supported by “National Natural Science Foundation of China (31800420, 31670541)”, “the Fundamental Research Funds for the Central Universities (WUT: 2018IB021)”, and “Nature Science Foundation of Hubei Province (2018CFB126, 2017CFB511)”.
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Xu, Z., Wu, Y., Xiao, Z. et al. Positive effects of Funneliformis mosseae inoculation on reed seedlings under water and TiO2 nanoparticles stresses. World J Microbiol Biotechnol 35, 81 (2019). https://doi.org/10.1007/s11274-019-2656-3
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DOI: https://doi.org/10.1007/s11274-019-2656-3