Skip to main content
SpringerLink
Log in

Arbuscular mycorrhizal fungi play a role in protecting roots of Sophora viciifolia Hance. from Pb damage associated with increased phytochelatin synthase gene expression

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Understanding the influence of arbuscular mycorrhizal (AM) fungi on the expressions of the dominant plant-related genes under heavy metal (HM) stress is important for developing strategies to reclaim polluted sites. In this study, we cloned full-length cDNAs of phytochelatin synthase gene (PCS1) and Actin of Sophora viciifolia Hance., a predominant plant in Qiandongshan lead and zinc mine, by rapid amplification of cDNA ends. Consequently, we studied the response of SvPCS1 to Funneliformis mosseae inoculation under lead stress (0, 50, and 200 μM Pb(NO3)2) at different durations (1, 3, and 7 days) using quantitative reverse-transcription polymerase chain-reaction (qRT-PCR) technique. The Pb concentrations and chlorophyll fluorescence parameters were also measured to assay Pb toxicity to Sophora viciifolia. We found that Pb concentrations in roots increased with increasing Pb application and the durations; the F v /F m , F v /F o , qP, and Y(II) decreased; NPQ rose with increasing Pb concentrations; mycorrhizal symbiosis alleviated the Pb toxicity to plants; and SvPCS1 was constitutively expressed in the roots. It was also found that F. mosseae inoculation could promote the expression of SvPCS1 with the concentration ≤200 μM at the exposure time shorter than 7 days.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

HMs:

Heavy metals

HM:

Heavy metal

PCs:

Phytochelatins

GSH:

Glutathione

PCS:

Phytochelatin synthases

F. mosseae :

Funneliformis mosseae

References

  • Assche FV, Clijsters H (2006) Effects of metals on enzyme activity in plants. Plant Cell Environ 13(3):195–206

    Article  Google Scholar 

  • Bilger W, Björkman O (1991) Temperature dependence of violaxanthin deepoxidation and non-photochemical fluorescence quenching in intact leaves of Gossypium hirsutum L. and Malvaparvi flora L. Planta 184:226–234

    Article  CAS  Google Scholar 

  • Bonanomi A, Wiemken A, Boller T, Salzer P (2001) Local induction of a mycorrhiza-specific class III chitinase gene in cortical root cells of Medicago truncatula containing developing or mature arbuscules. Plant Biol 3(2):194–199

    Article  CAS  Google Scholar 

  • Bu C-F, Liu G-B, Xu M-X (2003) Water potential of Sophora davidii in Loess Region of Shaanxi. Acta Bot Boreal-Occident Sin 23(8):1393–1397 (in Chinese)

    Google Scholar 

  • Cenkci S, Ciğerci İH, Yıldız M, Özay C, Bozdağ A, Terzi H (2010) Lead contamination reduces chlorophyll biosynthesis and genomic template stability in Brassica rapa L. Environ Exp Bot 67(3):467–473

    Article  CAS  Google Scholar 

  • Chen X, Wu C, Tang J, Hu S (2005) Arbuscular mycorrhizae enhance metal lead uptake and growth of host plants under a sand culture experiment. Chemosphere 60(5):665–671

    Article  CAS  Google Scholar 

  • Cheng SP (2003) Heavy metal pollution in China: origin, pattern and control. Environ Sci Pollut Res 10(3):192–198

    Article  CAS  Google Scholar 

  • Christophersen HM, Smith FA, Smith SE (2012) Unraveling the influence of arbuscular mycorrhizal colonization on arsenic tolerance in Medicago: Glomus mosseae is more effective than G. intraradices, associated with lower expression of root epidermal Pi transporter genes. Front Physiol 3:1–13

    Article  Google Scholar 

  • Cicatelli A, Lingua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S (2012) Arbuscular mycorrhizal fungi modulate the leaf transcriptome of a Populus alba L. clone grown on a zinc and copper-contaminated soil. Environ Exp Bot 75:25–35

    Article  CAS  Google Scholar 

  • Clemens S (2006) Evolution and function of phytochelatin synthases. J Plant Physiol 163(3):319–332

    Article  CAS  Google Scholar 

  • Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832

    Article  CAS  Google Scholar 

  • Cobbett CS, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  CAS  Google Scholar 

  • Dan TV, KrishnaRaj S, Saxena PK (2000) Metal tolerance of scented geranium (Pelargonium sp. “Frensham”): effects of cadmium and nickel on chlorophyll fluorescence kinetics. Int J Phytoremediat 2(1):91–104

    Article  CAS  Google Scholar 

  • Díaz G, Azcón-Aguilar C, Hornubia M (1996) Influence of arbuscular mycorrhizae on heavy metal (Zn and Pb) uptake and growth of Lygeum spartum and Anthyllis cystoides. Plant Soil 180:241–249

    Article  Google Scholar 

  • Ding Y, Wu SQ (2005) The peroxidase isozyme study of Sophora davidii and Sophora alopecuroides. J West China For Sci 34(3):67–68 (in Chinese)

    Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797

    Article  CAS  Google Scholar 

  • Estrella-Gómez NE, Mendoza-Cozatl D, Moreno-Sanchez R, Gonzalez-Mendoza D, Zapata-Perez O, Martinez-Hernandez A, Santamaria JM (2009) The Pb-hyperaccumulator aquatic fern Salvinia minima Baker, responds to Pb2+ by increasing phytochelatins via changes in SmPCS expression and in phytochelatin synthase activity. Aquat Toxicol 91(4):320–328

    Article  Google Scholar 

  • Figueroa ME, Fernández-Baco L, Luque T, Davy AJ (1997) Chlorophyll fluorescence, stress and survival in populations of Mediterranean grassland species. J Veg Sci 8:881–888

    Article  Google Scholar 

  • Garg N, Aggarwal N (2012) Effect of mycorrhizal inoculations on heavy metal uptake and stress alleviation of Cajanus cajan (L.) Millsp genotypes grown in cadmium and lead contaminated soils. Plant Growth Regul 66(1):9–26

    Article  CAS  Google Scholar 

  • Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F (2012) Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. Plant J 69(3):510–528

    Article  CAS  Google Scholar 

  • Ge L, Sun SB, Chen AQ, Kapulnik Y, Xu GH (2008) Tomato sugar transporter genes associated with mycorrhiza and phosphate. Plant Growth Regul 55(2):115–123

    Article  CAS  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochem Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Gong MG, Tang M, Chen H, Zhang QM, Feng XX (2013) Effects of two Glomus species on the growth and physiological performance of Sophora davidii seedlings under water stress. New For 44:399–408

    Article  Google Scholar 

  • González-Guerrero M, Azcón-Aguilar C, Ferrol N (2006) GintABC1 and GintMT1 are involved in Cu and Cd homeostasis in Glomus intraradices. In: Abstracts of the 5th international conference on Mycorrhiza, Granada, Spain

  • Grill ES, Winnacker E-L, Zenk MH (1985) Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science 230:674–676

    Article  CAS  Google Scholar 

  • Grill ES, Lӧffler S, Winnacker E-L, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamyldipeptidyl transpeptidase (phytochelatin synthase). Proc Natl Acad Sci U S A 86:6838–6842

    Article  CAS  Google Scholar 

  • 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(2):226–237

    Article  CAS  Google Scholar 

  • Guether M, Balestrini R, Hannah M, He J, Udvardi MK, Bonfante P (2009) Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol 182(1):200–212

    Article  CAS  Google Scholar 

  • Guimil S, Chang HS, Zhu T, Sesma A, Osbourn A, Roux C, Ionnidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP, Paszkowski U (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci U S A 102(22):8066–8070

    Article  Google Scholar 

  • Guo JL, Xu LP, Su YC, Wang HB, Gao SW, Xu JS, Que YX (2013) ScMT2-1-3, a metallothionein gene of sugarcane, plays an important role in the regulation of heavy metal tolerance/accumulation. Biomed Res Int. doi:10.1155/2013/904769

    Google Scholar 

  • Gupta M, Rai U, Tripathi R, Chandra P (1995) Lead induced changes in glutathione and phytochelatin in Hydrilla verticillata (l. f.) Royle. Chemosphere 30(10):2011–2020

    Article  CAS  Google Scholar 

  • Haneef I, Faizan S, Perveen R, Kausar S (2013) Role of arbuscular mycorrhizal fungi on growth and photosynthetic pigments in Coriandrum sativum L. grown under cadmium stress. World J Agric Sci 9(3):245–250

    Google Scholar 

  • Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42

    Article  CAS  Google Scholar 

  • Hoffmann T, Kutter C, Santamaria J (2004) Capacity of Salvinia minima Baker to tolerate and accumulate As and Pb. Eng Life Sci 4(1):61–65

    Article  CAS  Google Scholar 

  • Hogekamp C, Arndt D, Pereira PA, Becker JD, Hohnjec N, Kuster H (2011) Laser microdissection unravels cell-type-specific transcription in arbuscular mycorrhizal roots, including CAAT-box transcription factor gene expression correlating with fungal contact and spread. Plant Physiol 157(4):2023–2043

    Article  CAS  Google Scholar 

  • Howden R, Cobbett CS (1992) Cadmium-sensitive mutants of Arabidopsis thaliana. Plant Physiol 100:100–107

    Article  CAS  Google Scholar 

  • Huang GY, Wang YS (2010) Expression and characterization analysis of type 2 metallothionein from grey mangrove species (Avicennia marina) in response to metal stress. Aquat Toxicol 99(1):86–92

    Article  CAS  Google Scholar 

  • Islam E, Liu D, Li T, Yang X, Jin X, Mahmood Q, Tian S, Li J (2008) Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 154(1–3):914–926

    Article  CAS  Google Scholar 

  • Israr M, Jewell A, Kumar D, Sahi SV (2011) Interactive effects of lead, copper, nickel and zinc on growth, metal uptake and antioxidative metabolism of Sesbania drummondii. J Hazard Mater 186(2):1520–1526

    Article  CAS  Google Scholar 

  • Jarrah M, Ghasemi-Fasaei R, Karimian N, Ronaghi A, Zarei M, Mayel S (2014) Investigation of arbuscular mycorrhizal fungus and EDTA efficiencies on lead phytoremediation by sunflower in a calcareous soil. Bioremediat J 18(1):71–79

    Article  CAS  Google Scholar 

  • Khade SW, Adholeya A (2008) Effects of heavy metal (Pb) on arbuscular mycorrhizal fungi in vitro. World J Microbiol Biotechnol 24(9):1663–1668

    Article  CAS  Google Scholar 

  • Krajinski F, Hause B, Gianinazzi-Pearson V, Franken P (2002) Mtha1, a plasma membrane H+-ATPase gene from Medicago truncatula, shows arbuscule-specific induced expression in mycorrhizal tissue. Plant Biol 4(6):754–761

    Article  CAS  Google Scholar 

  • Kumar A, Prasad MN, Sytar O (2012) Lead toxicity, defense strategies and associated indicative biomarkers in Talinum triangulare grown hydroponically. Chemosphere 89(9):1056–1065

    Article  CAS  Google Scholar 

  • Leung H, Leung A, Ye Z, Cheung K, Yung K (2013) Mixed arbuscular mycorrhizal (AM) fungal application to improve growth and arsenic accumulation of Pteris vittata (As hyperaccumulator) grown in As-contaminated soil. Chemosphere 92(10):1367–1374

    Article  CAS  Google Scholar 

  • Li H, Cong Y, Wang HW, Sheng BL, Lin J, Chang YH (2010) Molecular cloning and expression analysis of a phytochelatin synthase gene, PcPCS1, from Pyrus calleryana Dcne. Acta Horticult Sin 37(6):880–891 (in Chinese)

    CAS  Google Scholar 

  • Liu JY, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15(9):2106–2123

    Article  CAS  Google Scholar 

  • Liu JY, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50(3):529–544

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408

    Article  CAS  Google Scholar 

  • Luo J (1987) Sophora davidii. Soil Water Conserv 6:38–39 (in Chinese)

    Google Scholar 

  • Marques APGC, Oliveira RS, Samardjieva KA, Pissarra J, Rangel AOSS, Castro PML (2007) Solanum nigrum grown in contaminated soil: effect of arbuscular mycorrhizal fungi on zinc accumulation and histolocalisation. Environ Pollut 145(3):691–699

    Article  CAS  Google Scholar 

  • Meier S, Azcon R, Cartes P, Borie F, Cornejo P (2011) Alleviation of Cu toxicity in Oenothera picensis by copper-adapted arbuscular mycorrhizal fungi and treated agrowaste residue. Appl Soil Ecol 48(2):117–124

    Article  Google Scholar 

  • Olsson PA, Thingstrup I, Jakobsen I, Baath E (1999) Estimation of the biomass of arbuscular mycorrhizal fungi in a linseed field. Soil Biol Biochem 31(13):1879–1888

    Article  CAS  Google Scholar 

  • Orłowska E, Godzik B, Turnau K (2012) Effect of different arbuscular mycorrhizal fungal isolates on growth and arsenic accumulation in Plantago lanceolata L. Environ Pollut 168:121–130

    Article  Google Scholar 

  • Ouziad F, Hildebrandt U, Schmelzer E, Bothe H (2005) Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. J Plant Physiol 162(6):634–649

    Article  CAS  Google Scholar 

  • Pandey N, Sharma CP (2002) Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage. Plant Sci 163(4):753–758

    Article  CAS  Google Scholar 

  • Pawlik-Skowrońska B (2002) Correlations between toxic Pb effects and production of Pb-induced thiol peptides in the microalga Stichococcus bacillaris. Environ Pollut 119(1):119–127

    Article  Google Scholar 

  • Phillips M, 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 55:158–161

    Article  Google Scholar 

  • Pichardo ST, Su Y, Han FX (2012) The potential effects of arbuscular mycorrhizae (AM) on the uptake of heavy metals by plants from contaminated soils. J Bioremediat Biodegrad. doi:10.4172/2155-6199.1000e124

    Google Scholar 

  • Piechalak A, Tomaszewska B, Baralkiewicz D, Malecka A (2002) Accumulation and detoxification of lead ions in legumes. Phytochemistry 60:153–162

    Article  CAS  Google Scholar 

  • Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. In: Whitacre DM (ed) Reviews of environmental contamination and toxicology, vol 213. Springer, New York, pp 113–136

    Google Scholar 

  • Prasas DDK, Prasas ARK (1987) Altered δ-aminolevulinic acid metabolism by lead and mercury in germinating seedlings of Bajra (Pennisetum typhoideum). J Plant Physiol 127(3–4):241–249

    Article  Google Scholar 

  • Punamiya P, Datta R, Sarkar D, Barber S, Patel M, Das P (2010) Symbiotic role of Glomus mosseae in phytoextraction of lead in vetiver grass [Chrysopogon zizanioides (L.)]. J Hazard Mater 177:465–474

    Article  CAS  Google Scholar 

  • Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414(6862):462–466

    Article  CAS  Google Scholar 

  • Rauser WE (1990) Phytochelatins. Ann Rev Biochem 59:61–86

    Article  CAS  Google Scholar 

  • Reddy AM, Kumar SG, Jyothsnakumari G, Thimmanaik S, Sudhakar C (2005) Lead induced changes in antioxidant metabolism of horsegram (Macrotyloma uniflorum (Lam.) Verdc.) and bengalgram (Cicer arietinum L.). Chemosphere 60(1):97–104

    Article  CAS  Google Scholar 

  • Rivera-Becerril F, Calantzis C, Turnau K, Caussanel JP, Belimov AA, Gianinazzi S, Strasser RJ, Gianinazzi-Pearson V (2002) Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes. J Exp Bot 53(371):1177–1185

    Article  CAS  Google Scholar 

  • Rivera-Becerril F, van Tuinen D, Martin-Laurent F, Metwally A, Dietz KJ, Gianinazzi S, Gianinazzi-Pearson V (2005) Molecular changes in Pisum sativum L. roots during arbuscular mycorrhiza buffering of cadmium stress. Mycorrhiza 16(1):51–60

    Article  CAS  Google Scholar 

  • Saba H, Jyoti P, Neha S (2013) Mycorrhizae and phytochelators as remedy in heavy metal contaminated land remediation. Int Res J Environ Sci 2(1):74–78

    Google Scholar 

  • Scarano G, Morelli E (2002) Characterization of cadmium- and lead-phytochelatin complexes formed in a marine microalga in response to metal exposure. BioMetals 15(2):145–151

    Article  CAS  Google Scholar 

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    Article  CAS  Google Scholar 

  • Sheng M, Tang M, Chen H, Yang BW (2008) Influence of arbuscular mycorrhizae on photosyntesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296

    Article  CAS  Google Scholar 

  • Singh RP, Tripathi RD, Sinha SK, Maheshwari R, Srivastava HS (1997) Response of higher plants to lead contaminated environment. Chemosphere 34(11):2467–2493

    Article  CAS  Google Scholar 

  • Singh RP, Tripathi RD, Dwivedi S, Kumar A, Trivedi P, Chakrabarty D (2010) Lead bioaccumulation potential of an aquatic macrophyte Najas indica are related to antioxidant system. Bioresour Technol 101(9):3025–3032

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Stobart AK, Griffiths WT, Ameen-Bukhari I, Sherwood RP (1985) The effect of Cd2+ on biosynthesis of chlorophyll in leaves of barley. Physiol Plant 63(3):293–298

    Article  CAS  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526

    CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599

    Article  CAS  Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Estimation of VA mycorrhizal infection levels in root systems. Research for estimation methods having a functional significance. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA Edition, Paris, pp 217–221

    Google Scholar 

  • Vestergaard M, Matsumoto S, Nishikori S, Shiraki K, Hirata K, Takagi M (2008) Chelation of cadmium ions by phytochelatin synthase: role of the cystein-rich C-terminal. Anal Sci 24:277–281

    Article  CAS  Google Scholar 

  • Vivares D, Arnoux P, Pignol D (2005) A papain-like enzyme at work: native and acyl-enzyme intermediate structures in phytochelatin synthesis. Proc Natl Acad Sci U S A 102(52):18848–18853

    Article  CAS  Google Scholar 

  • Volpe V, Dell'aglio E, Giovannetti M, Ruberti C, Costa A, Genre A, Guether M, Bonfante P (2013) An AM induced-MYB-family gene of Lotus japonicus (LjMAMI) affects root growth in an AM-independent manner. Plant J 73(3):442–455

    Article  CAS  Google Scholar 

  • Wang X, Zhou QX (2003) Distribution of forms for cadmium, lead, copper and zinc in soil land its influences by modifier. J Agric Environ Sci 22:541–545

    CAS  Google Scholar 

  • Wu SC, Cheung KC, Luo YM, Wong MH (2006) Effects of inoculation of plant growth-promoting rhizobacteria on metal uptake by Brassica juncea. Environ Pollut 140(1):124–135

    Article  CAS  Google Scholar 

  • Wulf A, Manthey K, Doll J, Perlick AM, Linke B, Bekel T, Meyer F, Franken P, Kuster H, Krajinski F (2003) Transcriptional changes in response to arbuscular mycorrhiza development in the model plant Medicago truncatula. Mol Plant Microbe Interact 16(4):306–314

    Article  CAS  Google Scholar 

  • Xu ZY, Tang M, Chen H, Ban YH, Zhang HH (2012) Microbial community structure in the rhizosphere of Sophora viciifolia grown at a lead and zinc mine of northwest China. Sci Total Environ 435–436:453–464

    Article  Google Scholar 

  • Zenk MH (1996) Heavy metal detoxification in higher plants-a review. Gene 179:21–30

    Article  CAS  Google Scholar 

  • Zhang XH, Zhu YG, Chen BD, Lin AJ, Smith SE, Smith FA (2005) Arbuscular mycorrhizal fungi contribute to resistance of upland rice to combined metal contamination of soil. J Plant Nutr 28(12):2065–2077

    Article  CAS  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 concentratioon. Eur J Soil Biol 46(5):306–311

    Article  Google Scholar 

  • Zhang XH, Wang YS, Lin AJ (2012) Effects of arbuscular mycorrhizal colonization on the growth of upland rice (Oryzal sativa L.) in soil experimentally contaminated with Cu and Pb. J Clin Toxicol. doi:10.4172/2161-0495.S3-003

    Google Scholar 

Download references

Acknowledgments

This research was supported by the National Natural Science Foundation of China (31270639, 31170607, and 31170567), Program for Changjiang Scholars and Innovative Research Team in University of China (IRT1035), and the Ph. D. Programs Foundation of Education Ministry of China (20100204110033, 20110204130001). We also thank Jennifer Forsythe (University of British Columbia) for her valuable suggestions to enhance the manuscript.

Author information

Authors and Affiliations

  1. State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Zhouying Xu & Ming Tang

  2. College of Forestry, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Yihui Ban, Zhen Li, Hui Chen, Ren Yang & Ming Tang

Authors
  1. Zhouying Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yihui Ban
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhen Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hui Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ren Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ming Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ming Tang.

Additional information

Responsible editor: Elena Maestri

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

(DOCX 333 kb)

Fig. S2

(DOCX 888 kb)

Fig. S3

(DOCX 634 kb)

Fig. S4

(DOCX 35 kb)

Table. S1

(DOCX 25 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, Z., Ban, Y., Li, Z. et al. Arbuscular mycorrhizal fungi play a role in protecting roots of Sophora viciifolia Hance. from Pb damage associated with increased phytochelatin synthase gene expression. Environ Sci Pollut Res 21, 12671–12683 (2014). https://doi.org/10.1007/s11356-014-3209-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3209-9

Keywords

Search

Navigation