摘要
本文采用变性梯度凝胶电泳(DGGE)技术,研究了陕西凤县铅硐山铅锌矿区优势植物狼牙刺(Sophora viciifolia Hance.)根际细菌和丛枝菌根(Arbuscular mycorrhizal,AM)真菌群落结构。利用透射电镜(TEM)、X射线能量散布分析仪(EDS)、实时荧光定量PCR(qRT-PCR)等技术,从球囊霉素螯合重金属、AM超微结构Pb定位、Pb胁迫下AM真菌对宿主植物络合素合酶基因表达的影响等方面探讨了AM真菌提高狼牙刺耐Pb性能的机制。主要结果如下:
1.铅锌矿区狼牙刺根际细菌群落结构
陕西凤县铅硐山铅锌矿区不同Pb污染程度的5个样地狼牙刺根际细菌多样性随着土壤污染程度的加剧而降低,DGGE图谱上的条带数从22个(污染程度最轻样地)降至13个(污染程度最严重样地)。土壤总Pb、有效Pb和细菌群落的香侬指数(H')极显著和显著负相关。Redundancy analysis(RDA)分析显示,土壤有效氮、有效Pb和有效磷对细菌群落结构影响较大,特征值分别为21.5%、17%和16.5%。从细菌DGGE胶上回收的15个条带中,11个属于变形菌门(Proteobacteria)中的不动杆菌属(Acinetobacter)、沙雷氏菌属(Serratia)和单胞菌属(Sphingomonas),3个属于厚壁菌门(Firmicutes)中的气球菌属(Aerococcus),1个属于放线菌属(Actinobacteria),优势细菌为变型菌门(Proteobacteria)。
2.铅锌矿区狼牙刺根际AM真菌群落结构及球囊霉素螯合重金属含量
不同Pb污染程度5个样地狼牙刺根系的AM真菌侵染率随着土壤Pb浓度的升高而降低。DGGE图谱上的条带数随着污染程度的加剧从31个降到13个。土壤中有效Pb含量与AM真菌的H'极显著负相关。RDA分析表明土壤总Pb、有效磷、有效氮和pH对AM真菌群落结构影响较大,特征值分别达到22.5%、20.1%、18.5%和6.2%。优势AM真菌为球囊霉科(Glomeraceae)球囊霉属(Glomus)和多孢囊霉科(Diversisporaceae)多孢囊霉属(Diversispora),在鉴定的13个序列中,10个属于球囊霉属(Glomus),2个属于多孢囊霉属(Diversispora),1个属于子囊菌门(Ascomycota)(非AM真菌)。
随着土壤Pb浓度的升高(57.5~6295.2mg/kg),总球囊霉素(GRSP)含量由2.9增加至6.8mg/g风干土,螯合的Pb含量为3.29~172.46mg/kg,占土壤Pb含量的2.74%~5.72%。GRSP螯合的Pb含量与土壤中总Pb、有效Pb含量分别极显著和显著正相关。球囊霉素在土壤中螯合Pb离子是AM真菌提高狼牙刺耐Pb的机制之一。
3. AM真菌对狼牙刺生长与吸Pb的影响及Pb在菌根超微结构中的定位
接种AM真菌摩西球囊霉(Glomus mosseae)于狼牙刺实生苗,结果显示,低浓度Pb(50μg/g)能够促进狼牙刺幼苗生长,高浓度Pb(500和1000μg/g)则抑制狼牙刺幼苗生长。接种G. mosseae降低了狼牙刺地上和地下部的Pb浓度,其中1000μg/gPb胁迫时,接种幼苗地上和地下部Pb浓度与对照相比降低了61.0%和15.2%。1000μg/g Pb胁迫时,接种幼苗的根长、根分叉数、根尖数、根表面积和根体积分别比对照提高220%、219%、157%、225%和278%。Pb胁迫下接种G. mosseae显著降低了直径0~0.2mm根长占总根长的百分比,而提高了直径0.4~0.6、0.6~0.8和0.8~1.0mm根长占总根长的百分比,即Pb胁迫条件下接种AM真菌有使根系变粗的趋势。
通过TEM和EDS技术对接种处理狼牙刺根系进行Pb的AM超微结构定位,发现Pb不仅能够沉积在狼牙刺根细胞内,还能沉积在AM真菌根内菌丝的细胞壁和空泡中,表明AM真菌在亚细胞水平上通过将重金属螯合在菌体细胞内从而增加狼牙刺的耐Pb能力。
4.狼牙刺植物络合素合酶及内参基因的克隆
通过Rapid-amplification of cDNA ends(RACE)方法克隆狼牙刺的植物络合素合酶基因(PCS1)及内参基因(Actin)。SvPCS1cDNA全长为2098bp,含有1503bp的开放阅读框(ORF),编码501个氨基酸,预测分子量为55.46kDa,等电点为7.13。SvPCS1编码的氨基酸序列与LjPCS1(百脉根,AAT80342)和GmPCS1(大豆,AAL78384)的同源性分别达到84.63%和85.43%。SvActin cDNA全长为1679bp,ORF为1134bp,编码378个氨基酸,预测分子量为41.65kDa,等电点为5.05。SvActin编码的氨基酸序列与RcActin(蓖麻,AAR15174)和TpActin(三叶草,AAQ74875)的同源性分别达到98.67%和98.42%。SvPCS1与SvActin的NCBI基因登录号分别为JQ780609和JQ780610。
5. Pb胁迫下AM真菌对狼牙刺植物络合素合酶基因表达的影响
通过Real-time quantitative PCR(qRT-PCR)技术,研究0、50和200μMPb(NO3)2胁迫1、3和7d后,接种G. mosseae对狼牙刺叶片叶绿素荧光参数、根系植物络合素合酶基因(SvPCS1)表达量和植物络合素(PCs)合成量的影响。结果显示,Pb胁迫后不接种处理狼牙刺叶片叶绿素荧光参数Fv/Fm、Fv/Fo、qP和Y(Ⅱ)随着Pb浓度的升高逐渐降低,NPQ随着Pb浓度的升高逐渐增加;接种处理各参数的变化趋势与不接种处理相同,但是变化幅度较小,说明接种G. mosseae缓解了植物所受Pb毒害。Pb胁迫1d和3d时,接种G. mosseae增加了狼牙刺根系SvPCS1的表达量和PCs的合成量,当胁迫7d时,0和50μM的Pb胁迫下接种处理SvPCS1的表达量和PCs的合成量仍然高于对照,200μM的Pb胁迫下低于对照,表明Pb胁迫一定时间和一定浓度内接种G. mosseae可以增加SvPCS1的表达量和PCs的合成量。
The arbuscular mycorrhizal (AM) fungal and bacterial community structures in therhizospere of the dominant plant Sophora viciifolia Hance. grown at Qiandongshan lead andzinc mine were investigated using PCR-DGGE. Using the technologies of transmissionelectron microscope (TEM), energy dispersive X-ray spectroscopy (EDS) and qutitativereverse transcription polymerase chain reaction (qRT-PCR), we discussed the mechnisms ofAM fungi improving S. viciifolia’s Pb resistance ability in the aspects of ultrastructurallocalization of Pb in AM, Pb chelation by glomalin related soil protein (GRSP) and the S.viciifolia phytochelatin synthase gene expression pattern impacted by AM fungi under Pbthreat. The main results are as follows:
1. The bacterial community structure in the rhizospere of S. viciifolia grown at fiveincreasing Pb concentration sites
In the five sites with increasing soil Pb concentration, the diversity of bacteria declinedwith increasing Pb concentration, the band number in DGGE profile decreased from22to13.Bacterial community H′was negatively correlated with the total and available Pbconcentrations in the soil. RDA analysis revealed that the available nitrogen, the available Pb,the available P affected the bacterial community mostly, with eigenvalues of21.5%,17%and16.5%, respectively. Among the fifteen species cloned from the gel, eleven wereAcinetobacter, Serratia and Sphingomonas in Proteobacteria; three were Aerococcus inFirmicutes and the other one was Actinobacteria in Actinobacteria.
2. The AM fungi community structure in the rhizospere of S. viciifolia grown at fiveincreasing Pb concentration sites and the heavy metal concentration chelated by glomalinrelated soil protein
AM root colonization decreased from30.5%to9.6%with the increase of the Pbconcentration in soil. The band number in the DGGE gel decreased from31to13. The H′ofthe AM fungal community showed a significant negative correlation with the available Pbconcentration The total soil Pb concentration, the available P, the available N and pH affectedthe AM fungi community structure mostly. The dominant AM fungi is Glomus in Glomeraceae and Diversispora in Diversisporaceae, among the thirteen sequences clonedfrom the gel, ten were Glomeraceae; two were Diversisporaceae and the other one was non-AM fungi.
Total GRSP (2.9~6.8mg/g dry soil) increased with the increase of the Pb concentration(57.5~6295.2mg/kg) in soil. The amount of Pb bound to GRSP varied from3.3to172.5mg/kg, which positively correlated with total and available soil Pb concentration, thus reducingthe bioavailability of Pb.
3. The influence of AM fungi inoculation on the growth and Pb uptake of S. viciifoliaand the Pb ultrastructure localization
The seedlings of S. viciifolia were inoculated with Glomus mosseae under different Pbappication levels, results showed low Pbconcentration (50μg/g) promoted the growth of S.viciifolia seedlings, but higher (500and1000μg/g) inhibited. Compared with non-inoculationtreatment, G. mosseae inoculation decreased both the Pb concentrations of aboveground andbelowground, the Pb concentrations of aboveground and belowground of the mycorrhizal S.viciifolia were118.48and47.49μg/g when exposed to1000μg/g Pb, decreased by61.0%and15.2%. The root length, root forks, root tips, root surface and root volumn of mycorrhizalS. viciifolia were higher than corresponding non-mycorrhizal plants. Compared with non-mycorrhizal plant, these parameters of mycorrhizal plants increased by220%、219%、157%、225%和278%when exposed to1000μg/g Pb(NO3)2. The ratio of root length whosediameters were between0~0.2mm to the total root length significantly increased with theincreasing Pb additions, and G. mosseae inoculation significantly reduced the ratio. Under Pbstress, G. mosseae increased the ratios of root length with0.4~0.6,0.6~0.8and0.8~1.0mmdiameters to the total root length, indicating that AM fungi inoculation thicken the roots with0.4~1.0mm diameter under Pb additions.
The combination data of TEM and EDS indicated that Pb can deposited not only in plantcells, but also the cell walls and vacuoles of the AM fungi intracellular hyphae, whichrevealling that the subcellular level mechanism of AM fungi alleviated the Pb toxicity to host.
4. Cloning the genes of SvPCS1and SvActin
The full length of SvPCS1cDNA is2098bp, containing a1503bp length ORF, coding501amino acids, predicted molecular weight is55.46kDa and the isoelectric point is7.13.The deduced amino acids of SvPCS1showed84.63%homology with LjPCS1(Lotusjaponicas, AAT80342), and85.43%with GmPCS1(Glycine max, AAL78384). The fulllength of SvActin cDNA is1679bp, including an1134bp length ORF, coding378aminoacids, predicted molecular weight is41.65kDa and the isoelectric point is5.05. Thehomology of SvActin with RcActin (Ricinus communis, AAR15174) and TpActin (Trifolium pretense, AAQ74875) reached98.67%and98.42%, respectively. The NCBI gene bankaccessing numbers of SvPCS1and SvActin are JQ780609and JQ780610, respectively.
5. The influence of AM fungi inoculation on SvPCS1expression
The response of SvPCS1expression, chlorophyll fluorescence parameters and phyto-chelatins (PCs) to G. mosseae inoculation under Pb stress (0,50and200μM Pb(NO3)2) atdifferent durations (1,3and7day) were studied. The chlorophyll fluorescence parametersFv/Fm, Fv/Fo, qP and Y(Ⅱ) of non-mycorrhizal S. viciifolia decreased and NPQ rose with theincreasing Pb concentration, all the parameters of mycorrhizal S. viciifolia showed the samechange patterns with non-mycorrhizal, but smaller change, indicating that mycorrhizalsymbiosis alleviated the Pb toxicity to plants. When S. viciifolia was exposed to0,50and200μM Pb for1and3d, G. mosseae inoculation promoted the expression of SvPCS1andsynthesis of PCs; when the duration increased to7d, SvPCS1expressions and PCs productionexposed to0and50μM Pb were still higher than controls, but lower in the S. viciifoliaexposed to200μM Pb, indicating that G. mosseae inoculation promoted SvPCS1expressionand SvPCs production under Pb threat for a certain period of time.
引文
丁锐,吴三桥.2005.苦豆子和狼牙刺过氧化物酶同工酶的研究.西部林业科学,34(3):67~68
郭学军,黄巧云,赵振华,陈雯莉.2002.微生物对土壤环境中重金属活性的影响.应用与环境生物学报,8(1):105~110
洪春来,魏幼璋,杨肖娥,贾彦博.2004.铅胁迫对蔬菜根系形态的影响研究.中国农学通报,20(5):176~177
候恩科,薛喜成,刘国民,马宗科,赵洲.2003.凤县矿山环境地质问题与保护对策.西北地质,36:26~30
黄化刚,李廷轩,杨肖娥,张锡洲,吴德勇.2009.植物对铅胁迫的耐性及其解毒机制研究进展.应用生态学报,20(3):696~704
何兰兰,角媛梅,王李鸿,周鸿斌.2009. Pb, Zn, Cu, Cd的超富集植物研究进展.环境科学与技术.32(11):120~123
贺学礼,张焕仕,赵丽莉.2008.不同土壤中水分胁迫和AM真菌对油蒿抗旱性的影响.植物生态学报,32(5):994~1001
李慧,从郁,王宏伟,盛宝龙,蔺经,常有宏.2010.豆梨植物络合素合酶PcPCS1基因克隆及其表达分析.园艺学报,37(6):880~890
栾静.2012.重金属胁迫下海州香薷根际微域细菌群落结构和特异基因表达研究[硕士学位论文].杭州:浙江大学.
刘润进,李晓林.2000.丛枝菌根及其应用.科学出版社.192~198
马洪明,路新枝,王勇.2002.四色荧光标记DNA序列中一例典型错读码的校正.海洋科学,26(3):10~12
牛振川.2012.秦岭凤县铅锌矿区AMF资源及耐铅性研究[硕士学位论文].杨凌:西北农林科技大学.
任光明,张琦,曲娟娟,闫立龙,孙兴滨.2012.铅锌矿区土壤细菌群落多样性分析.东北林业大学学报,40(1):58~61
孙海汐,王秀杰.2009. DNA测序技术发展及其展望. E-SCIENCE技术,6:24~26
王华丙,张振义,包锐.2007. ABC转运蛋白的结构与转运机制.生命的化学,27(3):208~210
王明元,夏仁学,王鹏.2010.丛枝菌根真菌对枳不同根围铁及球囊霉素螯合金属的影响.福建农林大学学报,39(1):42~46
王英辉,伍乃东.2007.铅污染土壤的植物修复技术研究.中国土壤与肥料,5:6~10
许冠东,2008. Genome Sequencer FLX引领快速基因组测序时代的到来.微生物学通报,35(1):149~151
姚善杰,田民民,武胜利.2004.陕西省凤县矿产资源开发和可持续发展.矿产与地质,18(5):470~475
张博,董瑜,袁建霞,张薇,张国.2012.土壤微生物区系国际研发态势分析.国际科技前沿报告.北京:科学出版社
张恩和,张新慧,王惠珍.2004.不同基因型春蚕豆对磷胁迫的适应性反应.生态学报,24(8):1589~1593
赵金莉,贺学礼.2011. AM真菌对白芷抗旱性和药用成分含量的影响.西北农业学报,20(3):184~189
赵旭东,魏东芝.2000.谷胱甘肽的简便测定法.药物分析杂志,20(1):34~37
Abdel-Latef A A H, He C X.2011. Arbuscular mycorrhizal influence on growth, photosynthetic pigments,osmotic adjustment and oxidative stress in tomato plants subjected to low temperature stress. ActaPhysiologiae Plantarum,33(4):1217~1225
Aguilera P, Borie F, Seguel A, Cornejo P.2011. Fluorescence detection of aluminum in arbuscularmycorrhizal fungal structures and glomalin using confocal laser scanning microscopy. Soil BiolBiochem,43(12):2427~2431
Aloui A, Recorbet G, Gollotte A, Robert F, Valot B, Gianinazzi-Pearson V, Aschi-Smiti S, Dumas-GaudotE.2009. On the mechanisms of cadmium stress alleviation in Medicago truncatula by arbuscularmycorrhizal symbiosis: A root proteomic study. Proteomics,9(2):420~433
Alscher R G.1989. Biosynthesis and antioxidant function of glutathione in plants. Physiol Plant,77(3):457~464
Andrade S A L, Grat o P L, Azevedo R A, Silveira A P D, Schiavinato M A, Mazzafera P.2010.Biochemical and physiological changes in jack bean under mycorrhizal symbiosis growing in soil withincreasing Cu concentrations. Environ Exp Bot,68(2):198~207
Andrade S A L, Grat o P L, Schiavinato M A, Silveira A P D, Azevedo R A, Mazzafera P.2009. Zn uptake,physiological response and stress attenuation in mycorrhizal jack bean growing in soil with increasingZn concentrations. Chemosphere,75(10):1363~1370
Arias J A, Peralta-Videa J R, Ellzey J T, Ren M H, Viveros M N, Gardea-Torresdey J L.2010. Effects ofGlomus deserticola inoculation on Prosopis: Enhancing chromium and lead uptake and translocationas confirmed by X-ray mapping, ICP-OES and TEM techniques. Environ Exp Bot,68(2):139~148
Arshad M, Silvestre J, Pinelli E, Kallerhoff J, Kaemmerer M, Tarigo A, Shahid M, Guiresse M, Pradère P,Dumat C.2008. A field study of lead phytoextraction by various scented Pelargonium cultivars.Chemosphere,71(11):2187~2192
Artursson V, Finlay R D, Jansson J K.2005. Combined bromodeoxyuridine immunocapture and terminal-restriction fragment length polymorphism analysis highlights differences in the active soil bacterialmetagenome due to Glomus mosseae inoculation or plant species. Environ Microbiol,7(12):1952~1966
Assche F V, Clijsters H.2006. Effects of metals on enzyme activity in plants. Plant Cell Environ,13(3):195~206
Audet P, Charest C.2006. Effects of AM colonization on "wild tobacco" plants grown in zinc-contaminated soil. Mycorrhiza16:277~283
Audet P, Charest C.2012. Assessing arbuscular mycorrhizal plant metal uptake and soil metalbioavailability among "dwarf" sunflowers in a stratified compartmental growth environment. ArchivesAgron Soil Sci,59(4):533~548
Bago B, Pfeffer P E, Shachar-Hill Y.2000. Carbon metabolism and transport in arbuscular mycorrhizas.Plant Physiol,124(3):949~957
Bago B, Vierheilig H, Piche Y, AzconAguilar C.1996. Nitrate depletion and pH changes induced by theextraradical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown in monoxenicculture. New Phytologist,133(2):273~280
Bao Q S, Lu C Y, Song H, Wang M, Ling W H, Chen W Q, Deng X Q, Hao Y T, Rao S Q.2009.Behavioural development of school-aged children who live around a multi-metal sulphide mine inGuangdong province, China: a cross-sectional study. BMC Public Health,9(1):217~224
Becerra-Castro C, Kidd P S, Prieto-Fernandez A, Weyens N, Acea M-J, Vangronsveld J.2011. Endophyticand rhizoplane bacteria associated with Cytisus striatus growing on hexachlorocyclohexane-contaminated soil: isolation and characterisation. Plant Soil,340(1-2):413~433
Bedini S, Argese E, Gobbo L, Pietrangeli B, Giovannetti M.2009. Metalli pesanti nei suoli: il possibileruolo dei funghi micorrizici arbuscolari. Ambiente Risorse Salute,121:13~16
Bedini S, Turrini A, Rigo C, Argese E, Giovannetti M.2010. Molecular characterization and glomalinproduction of arbuscular mycorrhizal fungi colonizing a heavy metal polluted ash disposal island,downtown Venice. Soil Biol Biochem,42:758~765
Belimov A A, Safronova V I, Sergeyeva T A, Egorova T N, Matveyeva V A, Tsyganov V E.2001.Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol,47(7):642~652
Beyene S, Ricken B, Hofner W.1996. Effects of arbuscular mycorrhizal fungus on dry matter yield, as wellas P and K concentrations in Maize (Zea mays L.) at increasing levels of P supply. J Appl Bot-AngewBot,70(5-6):194~198
Bhuiyan M S U, Min S R, Jeong W J, Sultana S, Choi K S, Lee Y, Liu J R.2011. Overexpression ofAtATM3in Brassica juncea confers enhanced heavy metal tolerance and accumulation. Plant Cell TissOrg,107(1):69~77
Bilger W, Bj rkman O.1991. Temperature dependence of violaxanthin deepoxidation and nonphoto-chemical fluorescence quenching in intact leaves of Gossypium hirsutum L. and Malvaparvi flora L.Planta,184:226~234
He B, Yun Z J, Shi J B, Jiang G B.2013. Research progress of heavy metal pollution in China: Sources,analytical methods, status, and toxicity. Chin Sci Bull,58(2):134~140
Bird S B, Herrick J E, Wander M M, Wright S F.2002. Spatial heterogeneity of aggregate stability and soilcarbon in semi-arid rangeland. Environ Pollut,116(3):445~455
Boivin M E Y, Greve G D, García-Meza J V, Massieux B, Sprenger W, Kraak M H S, Breure A M,Rutgers M, Admiraal W.2007. Algal-bacterial interactions in metal contaminated floodplainsediments. Environ Pollut,145(3):884~894
Bovet L, Eggmann T, Meylan-Bettex M, Polier J, Kammer P, Marin E, Feller U, Martinoia E.2003.Transcript levels of AtMRPs after cadmium treatment: induction of AtMRP3. Plant Cell Environ,26(3):371~381
Braud A, Jézéquel K, Vieille E, Tritter A, Lebeau T.2006. Change in extractability of Cr and Pb in apolycontaminated soil after bioaugmentation with microbial producers of biosurfactants, organic acidsand siderophores. Water Air Soil Poll,6:261~279
Breuninger M, Trujillo C G, Serrano E, Fischer R, Requena N.2004. Different nitrogen sources modulateactivity but not expression of glutamine synthetase in arbuscular mycorrhizal fungi. Fungal Genet Biol,41(5):542~552
Burleigh S H, Kristensen B K, Bechmann I E.2003. A plasma membrane zinc transporter from Medicagotruncatula is up-regulated in roots by Zn fertilization, yet down-regulated by arbuscular mycorrhizalcolonization. Plant Mol Biol,52(5):1077~1088
Camprubi A, Abril M, Estaun V, Calvet C.2012. Contribution of arbuscular mycorrhizal symbiosis to thesurvival of psammophilic plants after sea water flooding. Plant Soil,351(1-2):97~105
Casamayor E O, Schafer H, Baneras L, Pedros-Alio C, Muyzer G.2000. Identification of and spatio-temporal differences between microbial assemblages from two neighboring sulfurous lakes:comparison by microscopy and denaturing gradient gel electrophoresis. Appl Environ Microbiol,66:499~508
Castiglione S, Todeschini V, Franchin C, Torrigiani P, Gastaldi D, Cicatelli A, Rinaudo C, Berta G, BiondiS, Lingua G.2009. Clonal differences in survival capacity, copper and zinc accumulation, andcorrelation with leaf polyamine levels in poplar: A large-scale field trial on heavily polluted soil.Environ Pollut,157(7):2108~2117
Cenkci S, Ci erci H, Y ld z M, zay C, Bozda A, Terzi H.2010. Lead contamination reduceschlorophyll biosynthesis and genomic template stability in Brassica rapa L. Environ Exp Bot,67(3):467~473
Chen H M, Muramoto K, Yamauchi F, Nokihara K.1996. Antioxidant activity of designed pepeides basedon the antioxidative peptide isolated from digests of a soybean protein. J Agric Food Chem,44:2619~2623
Chen X, Tang J J, Zhi G Y, Hu S J.2005a. Arbuscular mycorrhizal colonization and phosphorusacquisition of plants: effects of coexisting plant species. Appl Soil Ecol,28(3):259~269
Chen X, Wu C, Tang J, Hu S.2005b. Arbuscular mycorrhizae enhance metal lead uptake and growth ofhost plants under a sand culture experiment. Chemosphere,60(5):665~671
Chern E, Tsai D, Ogunseitan O.2007. Deposition of glomalin-related soil protein and sequestered toxicmetals into watersheds. Environ Sci Technol,41:3566~3572
Christensen H, Jakobsen I.1993. Reduction of bacterial growth by a vesicular-arbuscular mycorrhizalfungus in the rhizosphere of cucumber (Cucumis sativus L.). Biol Fert Soils,15:253~258
Christophersen H M, Smith F A, Smith S E.2012. Unraveling the influence of arbuscular mycorrhizalcolonization on arsenic tolerance in Medicago: Glomus mosseae is more effective than G. intraradices,associated with lower expression of root epidermal Pi transporter genes. Front Physio, doi:10.3389/fphys.2012.00091
Cicatelli A, Lingua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S.2012. Arbuscular mycorrhizalfungi modulate the leaf transcriptome of a Populus alba L. clone grown on a zinc and copper-contaminated soil. Environ Exp Bot,75:25~35
Citterio S, Prato N, Fumagalli P, Aina R, Massa N, Santagostino A, Sgorbati S, Berta G.2005. Thearbuscular mycorrhizal fungus Glomus mosseae induces growth and metal accumulation changes inCannabis sativa L. Chemosphere,59(1):21~29
Clemens S.2006. Evolution and function of phytochelatin synthases. J Plant Physiol,163(3):319~332
Clemens S, Kim E J, Neumann D, Schroeder J I.1999. Tolerance to toxic metals by a gene family ofphytochelatin synthases from plants and yeast. EMBO J,18(12):3325~3333
Cobbett C S, Goldsbrough P.2002. Phytochelatins and metallothioneins: roles in heavy metal detoxi-fication and homeostasis. Annu Rev Plant Biol,53:159~182
Cobbett C S.1999. A family of phytochelatin synthase genes from plant, fungal and animal species. TrendsPlant Sci,4(9):335~337
Cobbett C S.2000. Phytochelatins and their roles in heavy metal detoxification. Plant Physiol,123(3):825~832
Conte S S, Walker E L.2011. Transporters contributing to iron trafficking in plants. Mol Plant,4(3):464~476
Cornejo P, Meier S, Borie G, Rillig M C, Borie F.2008. Glomalin-related soil protein in a Mediterraneanecosystem affected by a copper smelter and its contribution to Cu and Zn sequestration. Sci TotalEnviron,406(1-2):154~160
Dabrowska G, Hrynkiewicz K, Trejgell A.2012. Do arbuscular mycorrhizal fungi affect metallothioneinMT2expression in Brassica Napus L. roots? Acta Biol Cracov Ser Bot,54(1):34~39
Dan T V, KrishnaRaj S, Saxena P K.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
Daniell T J, Husband R, Fitter A H, Young J P W.2001. Molecular diversity of arbuscualr mycorrhizalfungi colonising arable crops. FEMS Microbiol Ecol,36:203~209
De la Iglesia R, Valenzuela-Heredia D, Andrade S, Correa J, Gonzalez B.2012. Composition dynamics ofepilithic intertidal bacterial communities exposed to high copper levels. FEMS Microbiol Ecol,79(3):720~727
Demmig-Adams B, Adams W W, Barker D H, Logan B A, Bowling D R, Verhoeven A S.1996. Usingchlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation ofexcess excitation. Physiol Plant,98(2):253~264
Dey S K, Dey J, Patra S, Pothal D.2007. Changes in the antioxidative enzyme activities and lipidperoxidation in wheat seedlings exposed to cadmium and lead stress. Brazilian J Plant Physiol,19(1):53~60
D az G, Azcón-Aguilar C, Hornubia M.1996. Influence of arbuscular mycorrhizae on heavy metal (Zn andPb) uptake and growth of Lygeum spartum and Anthyllis cystoides. Plant Soil,180:241~249
Dickie I A, FitzJohn R G.2007. Using terminal restriction fragment length polymorphism (T-RFLP) toidentify mycorrhizal fungi: a methods review. Mycorrhiza,17(4):259~270
Dong W Q Y, Cui Y, Liu X.2001. Instances of soil and crop heavy metal contamination in China. SoilSediment Contam,10(5):497~510
Dueck T A, Visser P, Ernst W H O, Schat H.1986. Vesicular-arbuscular mycorrhizae decrease zinc-toxicity to grasses growing in zinc-polluted soil. Soil Biol Biochem,18(3):331~333
Dumbrell A J, Ashton P D, Aziz N, Feng G, Nelson M, Dytham C, Fitter A H, Helgason T.2011. Distinctseasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing.New Phytol,190(3):794~804
Edgar R C.2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. NucleicAcids Res,32(5):1792~1797
Estrella-Gómez N E, Sauri-Duch E, Zapata-Pérez O, Santamaría J M.2012. Glutathione plays a role inprotecting leaves of Salvinia minima from Pb2+damage associated with changes in the expression ofSmGS genes and increased activity of GS. Environ Exp Bot,75:188~194
Estrella-Gomez N E, Mendoza-Cozatl D, Moreno-Sanchez R, Gonzalez-Mendoza D, Zapata-Perez O,Martinez-Hernandez A, Santamaria J M.2009. The Pb-hyperaccumulator aquatic fern Salviniaminima Baker, responds to Pb(2+) by increasing phytochelatins via changes in SmPCS expression andin phytochelatin synthase activity. Aquat Toxicol,91(4):320~328
Eun S-O, Shik-Youn H, Lee Y.2008. Lead disturbs microtubule organization in the root meristem of Zeamays. Physiol Plant,110(3):357~365
Ezawa T, Cavagnaro T R, Smith S E, Smith F A, Ohtomo R.2004. Rapid accumulation of polyphosphatein extraradical hyphae of an arbuscular mycorrhizal fungus as revealed by histochemistry and apolyphosphate kinase/luciferase system. New Phytol,161(2):387~392
Fellbaum C R, Gachomo E W, Beesetty Y, Choudhari S, Strahan G D, Pfeffer P E, Kiers E T, Bucking H.2012. Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizalsymbiosis. Proc Natl Acad Sci USA,109(7):2666~2671
Feris K, Ramsey P, Frazar C, Moore J N, Gannon J E, Holben W E.2003. Differences in hyporheic-zonemicrobial community structure along a heavy-metal contamination gradient. Appl Environ Microbiol,69(9):5563~5573
Ferrol N, González-Guerrero M, Valderas A, Benabdellah K, Azcón-Aguilar C.2009. Survival strategies ofarbuscular mycorrhizal fungi in Cu-polluted environments. Phytochem Rev,8(3):551~559
Fierer N, Schimel P J, Holden P A.2003. Variations in microbial community composition through two soildepth profiles. Soil Biol Biochem,35:167~176
Fitter A H, Helgason T, Hodge A.2011. Nutritional exchanges in the arbuscular mycorrhizal symbiosis:implications for sustainable agriculture. Fungal Biol Rev,25(1):68~72
Fu B J.2008. Blue skies for China. Science,321(5889):611~611
Gasic K, Korban S S.2007. Transgenic Indian mustard (Brassica juncea) plants expressing an Arabidopsisphytochelatin synthase (AtPCS1) exhibit enhanced As and Cd tolerance. Plant Mol Biol,64(4):361~369
Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F.2012. Arbuscule-containing and non-colonizedcortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscularmycorrhizal development. Plant J,69(3):510~528
Genty B, Briantais J M, Baker N R.1989. The relationship between the quantum yield of photosyntheticelectron transport and quenching of chlorophyll fluorescence. Biochem Biophys Acta,990:87~92
Gildon A, Tinker P.1983. Interactions of vesicular arbuscular mycorrizal infection and heavy metals inplants. I. The effects of heavy metals on the development of vesicular-arbuscular mycorrhizas. NewPhytol.95:947~961
Gillespie A W, Farrell R E, Walley F L, Ross A R S, Leinweber P, Eckhardt K-U, Regier T Z, Blyth R I R.2011. Glomalin-related soil protein contains non-mycorrhizal-related heat-stable proteins, lipids andhumic materials. Soil Biol Biochem,43(4):766~777
Glick B R, Patten C L, Holguin G, Penrose D M.1999. Biochemical and genetic mechanisms used by plantgrowth promoting bacteria. London: Imperial College Press.
Gollotte A, Van-Tuinen D, Atkinson D.2004. Diversity of arbuscular mycorrhizal fungi colonising roots ofthe grass species Agrostis capillaris and Lolium perenne in a field experiment. Mycorrhiza,14(2):111~117
González-Chavez M C, Carrillo-González R, Wright S F, Nichols K A.2004. The role of glomalin, aprotein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. EnvironPollut,130(3):317~323
González-Guerrero M, Azcón-Aguilar C, Mooney M, Valderas A, MacDiarmid C W, Eide D J, Ferrol N.2005. Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cationdiffusion facilitator family. Fungal Genet Biol,42(2):130~140
González-Guerrero M, Azcón-Aguilar C, Ferrol N.2006. GintABC1and GintMT1are involved in Cu andCd homeostasis in Glomus intraradices. In: Abstracts of the5thinternational conference onMycorrhiza, Granada, Spain.
Gopal R, Rizvi A H.2008. Excess lead alters growth, metabolism and translocation of certain nutrients inradish. Chemosphere,70(9):1539~1544
Gorzelak M A, Hambleton S, Massicotte H B.2012. Community structure of ericoid mycorrhizas and root-associated fungi of Vaccinium membranaceum across an elevation gradient in the Canadian RockyMountains. Fungal Ecol,5(1):36~45
Grill E, L ffler S, Winnacker E-L, Zenk M H.1989. Phytochelatins, the heavy-metal-binding peptides ofplants, are synthesized from glutathione by a specific γ-glutamyldipeptidyl transpeptidase(phytochelatin synthase). Proc Natl Acad Sci USA,86:6838~6842
Grill E, Winnacker E L, Zenk M H.1987. Phytochelatins, a class of heavy-metal-binding peptides fromplants, are functionally analogous to metallothioneins. Proc Nat Acad Sci USA,84(2):439~443
Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G.2010. Expression analysis suggests potential roles ofmicroRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. PhysiolPlant,138(2):226~237
Guo W J, Meetam M, Goldsbrough P B.2008. Examining the specific contributions of individualArabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiol,146(4):1697~1706
Gupta D K, Nicoloso F T, Schetinger M R C, Rossato L V, Pereira L B, Castro G Y, Srivastava S, TripathiR D.2009. Antioxidant defense mechanism in hydroponically grown Zea mays seedlings undermoderate lead stress. J Hazard Mater,172(1):479~484
Gupta M, Rai U, Tripathi R, Chandra P.1995. Lead induced changes in glutathione and phytochelatin inHydrilla verticillata (l. f.) Royle. Chemosphere,30(10):2011~2020
Hall J L.2002. Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot,53(366):1~11
Harley J L, Harley E L.1987. A check-list of mycorrhiza in the British flora. New Phytol,105(2):1~102
Harrison M J.2005. Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol,59:19~42
Hassan S E D, Boon E, St-Arnaud M, Hijri M.2011. Molecular biodiversity of arbuscular mycorrhizalfungi in trace metal-polluted soils. Mol Ecol,20(16):3469~3483
He Z Y, Li J C, Zhang H Y, Ma M.2005. Different effects of calcium and lanthanum on the expression ofphytochelatin synthase gene and cadmium absorption in Lactuca sativa. Plant Sci,168(2):309~318
Helgason T, Daniell T J, Husband R, Fitter A H, Young J P.1998. Ploughing up the wood-wide web?Nature,394(6692):431
Hildebrandt U, Regvar M, Bothe H.2007. Arbuscular mycorrhiza and heavy metal tolerance.Phytochemistry,68(1):139~146
Hoffmann T, Kutter C, Santamaria J.2004. Capacity of Salvinia minima Baker to tolerate and accumulateAs and Pb. Eng Life Sci,4(1):61~65
Howden R, Cobbett C S.1992. Cadmium-sensitive mutants of Arabidopsis thaliana. Plant Physiol,100:100~107
Howden R, Goldsbrough P B, Andersen C R, Cobbett C S.1995. Cadmium-sensitive, cad1mutants ofArabidopsis thaliana are deficient. Plant Physiol,107:1059~1066
Huang G Y, Wang Y S.2010. Expression and characterization analysis of type2metallothionein from greymangrove species (Avicennia marina) in response to metal stress. Aqua Toxicol,99(1):86~92
Inouhe M.2005. Phytochelatins. Brazilian J Plant Physiol,17(1):65~78
Islam E, Liu D, Li T Q, Yang X E, Jin X F, Mahmood Q, Tian S K, Li J Y.2008. Effect of Pb toxicity onleaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater,154(1-3):914~926
Islam E, Yang X E, Li T Q, Liu D, Jin X F, Meng F H.2007. Effect of Pb toxicity on root morphology,physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater,147(3):806~816
Israr M, Jewell A, Kumar D, Sahi S V.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
Jamal A, Ayub N, Usman M, Khan D A G.2002. Arbuscular mycorrhizal fungi enhance zinc and nickeluptake from contaminated soil by soybean and lentil. Int J Phytoremediat,4(3):205~221
Javot H, Penmetsa R V, Terzaghi N, Cook D R, Harrison M J.2007. A Medicago truncatula phosphatetransporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA,104(5):1720~1725
Jeong S, Moon H S, Nam K, Kim J Y, Kim T S.2012. Application of phosphate-solubilizing bacteria forenhancing bioavailability and phytoextraction of cadmium (Cd) from polluted soil. Chemosphere,88(2):204~210
Jiang W S, Liu D H.2010. Pb-induced cellular defense system in the root meristematic cells of Alliumsativum L. BMC Plant Biol,10(1):1~8
Jin H Y, Germida J J, Walley F L.2013. Impact of arbuscular mycorrhizal fungal inoculants on subsequentarbuscular mycorrhizal fungi colonization in pot-cultured field pea (Pisum sativum L.). Mycorrhiza,23(1):45~59
Keltjens W G, Van-Beusichem M L.1998. Phytochelatins as biomarkers for heavy metal stress in maize(Zea mays L.) and wheat (Triticum aestivum L.): combined effects of copper and cadmium. Plant Soil,203(1):119~126
Kim D Y, Bovet L, Kushnir S, Noh E W, Martinoia E, Lee Y.2006. AtATM3is involved in heavy metalresistance in Arabidopsis. Plant Physiol,140(3):922~932
Kneer R, Zenk M H.1992. Phytochelatins protect plant enzymes from heavy metal poisoning.Phytochemistry,31(8):2663~2667
Kopittke P M, Asher C J, Kopittke R A, Menzies N W.2007. Toxic effects of Pb2+on growth of cowpea(Vigna unguiculata). Environ Pollut,150(2):280~287
Kr mer U.2005. Phytoremediation: novel approaches to cleaning up polluted soils. Curr Opin Biotechnol,16(2):133~141
Krajinski F, Hause B, Gianinazzi-Pearson V, Franken P.2002. Mtha1, a plasma membrane H+-ATPasegene from Medicago truncatula, shows arbuscule-specific induced expression in mycorrhizal tissue.Plant Biology,4(6):754~761
Kruger M, Stockinger H, Kruger C, Schussler A.2009. DNA-based species level detection ofGlomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol,183(1):212~223
Kuar G, Singh H P, Batish D R, Kohli R K.2013. Lead (Pb)-induced biochemical and ultrastructuralchanges in wheat (Triticum aestivum) roots. Protoplasma, doi:10.1007/s00709-011-0372-4
Kuffner M, De Maria S, Puschenreiter M, Fallmann K, Wieshammer G, Gorfer M, Strauss J, Rivelli A R,Sessitsch A.2010. Culturable bacteria from Zn-and Cd-accumulating Salix caprea with differentialeffects on plant growth and heavy metal availability. J Appl Microbiol,108(4):1471~1484
Kumar A, Prasad M N V, Sytar O.2012. Lead toxicity, defense strategies and associated indicativebiomarkers in Talinum triangulare grown hydroponically. Chemosphere,89(9):1056~1065
Lanfranco L, Bolchi A, Ros E C, Ottonello S, Bonfante P.2002. Differential expression of ametallothionein gene during the presymbiotic versus the symbiotic phase of an arbuscular mycorrhizalfungus. Plant Physiol,130(1):58~67
Lee J, Lee S, Young J P.2008. Improved PCR primers for the detection and identification of arbuscularmycorrhizal fungi. FEMS Microbiol Ecol,65(2):339~349
Lee M, Lee K, Lee J, Noh E W, Lee Y.2005. AtPDR12contributes to lead resistance in Arabidopsis. PlantPhysiol,138(2):827~836
Lekberg Y, Schnoor T, Kjoller R, Gibbons S M, Hansen L H, Al-Soud W A, Sorensen S J, Rosendahl S.2012.454-sequencing reveals stochastic local reassembly and high disturbance tolerance withinarbuscular mycorrhizal fungal communities. J Ecol,100(1):151~160
Leopold I, Gunther D, Schmidt J, Neumann D.1999. Phytochelatins and heavy metal tolerance.Phytochemistry,50(8):1323~1328
Leung H M, Ye Z H, Wong M H.2006. Interactions of mycorrhizal fungi with Pteris vittata (Ashyperaccumulator) in As-contaminated soils. Environ Pollut,139(1):1~8
Li X L, Christie P.2001. Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizalred clover in Zn-contaminated soil. Chemosphere,42(2):201~207
Li Y J, Dhankher O P, Carreira L, Lee D, Chen A, Schroeder J I, Balish R S, Meagher R B.2004.Overexpression of phytochelatin synthase in Arabidopsis leads to enhanced arsenic tolerance andcadmium hypersensitivity. Plant Cell Physiol,45(12):1787~1797
Li Z S, Lu Y P, Zhen R G, Szczypka M, Thiele D J, Rea P A.1997. A new pathway for vacuolar cadmiumsequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis (glutathionato) cadmium.Proceed Nat Acad Sci USA,94(1):42~47
Liao G L.2008. Assessment of soil heavy metal pollution in different mining zones of a nonferrous metalmine. Archives Environ Prot,34(4):93~100
Lim Y W, Kim B K, Kim C, Jung H S, Kim B S, Lee J H, Chun J.2010. Assessment of soil fungalcommunities using pyrosequencing. J Microbiol,48(3):284~289
Ling Q F, Hong F S.2009. Effects of Pb2+on the structure and function of Photosystem II of Spirodelapolyrrhiza. Biol Trace Elem Res,129(1):251~260
Liu D, Li T Q, Jin X F, Yang X E, Islam E, Mahmood Q.2008. Lead induced changes in the growth andantioxidant metabolism of the lead accumulating and non‐accumulating ecotypes of Sedum alfredii. JIntegr Plant Biol,50(2):129~140
Liu Y, Zhu Y G, Chen B D, Christie P, Li X L.2005. Influence of the arbuscular mycorrhizal fungusGlomus mosseae on uptake of arsenate by the As hyperaccumulator fern Pteris vittata L. Mycorrhiza,15(3):187~192
Liu Z, Gu C, Chen F, Yang D, Wu K, Chen S, Jiang J, Zhang Z.2012. Heterologous expression of aNelumbo nucifera phytochelatin synthase gene enhances cadmium tolerance in Arabidopsis thaliana.Appl Biochem Biotechnol,166(3):722~734
Livak K J, Schmittgen T D.2001. Analysis of relative gene expression data using real-time quantitativePCR and the2(-Delta Delta C(T)) method. Methods,25(4):402~408
Loeffler S, Hochberger A, Grill E, Winnacker E L, Zenk M H.1989. Termination of the phytochelatinsynthase reaction through sequestration of heavy metals by the reaction product. FEBS Lett,258(1):42~46
Long L K, Yao Q, Guo J, Yang R H, Huang Y H, Zhu H H.2010. Molecular community analysis ofarbuscular mycorrhizal fungi associated with five selected plant species from heavy metal pollutedsoils. Euro J Soil Biol,46(5):288~294
Lopez-Pedrosa A, Gonzalez-Guerrero M, Valderas A, Azcon-Aguilar C, Ferrol N.2006. GintAMT1encodes a functional high-affinity ammonium transporter that is expressed in the extraradicalmycelium of Glomus intraradices. Fungal Genet Biol,43(2):102~110
Lovelock C E, Wright S F, Clark D A, Ruess R W.2004. Soil stocks of glomalin produced by arbuscularmycorrhizal fungi across a tropical rain forest landscape. J Ecol,92(2):278~287
Malcová R, Vosátka M, Gryndler M.2003. Effects of inoculation with Glomus intraradices on lead uptakeby Zea mays L. and Agrostis capillaris L. Appl Soil Ecol,23(1):55~67
Maldonado-Mendoza I E, Dewbre G R, Harrison M J.2001. A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response tophosphate in the environment. Mol Plant Microbe Interaction,14(10):1140~1148
Mantel N.1967. The detection of disease clustering and a generalized regression approach. Cancer Res,27:209~220
Ma Y, Rajkumar M, Luo Y M, Freitas H.2011. Inoculation of endophytic bacteria on host and non-hostplants-effects on plant growth and Ni uptake. J Hazard Mater,195:230~237
Marques A P G C, Oliveira R S, Samardjieva K A, Pissarra J, Rangel A O S S, Castro P M L.2007.Solanum nigrum grown in contaminated soil: Effect of arbuscular mycorrhizal fungi on zincaccumulation and histolocalisation. Environ Pollut,145:691~699
Mehra R K, Mulchandani P.1995. Glutathione-mediated transfer of Cu (I) into phytochelatins. Biochem J,307(Pt3):697~705
Meier S, Azcón R, Cartes P, Borie F, Cornejo P.2011. Alleviation of Cu toxicity in Oenothera picensis bycopper-adapted arbuscular mycorrhizal funi and treated agrowaste rsidue. Appl Soil Ecol,48(2):117~124
Meier S, Borie F, Bolan N, Cornejo P.2012. Phytoremediation of metal-polluted soils by arbuscularmycorrhizal fungi. Crit Rev Env Sci Tec,42(7):741~775
Merryweather J, Fitter A.1998. The arbuscular mycorrhizal fungi of Hyacinthoides non-scripta I. Diversityof fungal taxa. New Phytol,138(1):117~129
Mishra S, Srivastava S, Tripathi R D, Kumar R, Seth C S, Gupta D K.2006. Lead detoxification bycoontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system inresponse to its accumulation. Chemosphere,65(6):1027~1039
Mohammad A, Mittra B.2013. Effects of inoculation with stress-adapted arbuscular mycorrhizal fungusGlomus deserticola on growth of Solanum melogena L. and Sorghum sudanese Staph. seedlings undersalinity and heavy metal stress conditions. Archives Agron Soil Sci,59(2):173~183
Morton J B, Redecker D.2001. Two new families of Glomales, Archaeosporaceae and Paraglomaceae,with two new genera Archaeospora and Paraglomus, based on concordant molecular andmorphological characters. Mycologia,93(1):181~195
Mroczek-Zdyrska M, Wójcik M.2012. The influence of selenium on root growth and oxidative stressinduced by lead in Vicia faba L. minor plants. Biol Trace Elem Res,147:320~328
Murasugi A, Hayashi Y.1981. Cadmium-binding peptide induced in fission yeast, Schizosaccharomycespombe. J Biochem,90(5):1561~1565
Muyzer G, de-Waal E C, Uitterlinden A G.1993. Profiling of complex microbial populations by denaturinggradient gel electrophoresis analysis of polymerase chain reaction-amplified gene coding for16SrRNA. Appl Environ Microbiol,59(3):695~700
Or owska E, Godzik B, Turnau K.2012. Effect of different arbuscular mycorrhizal fungal isolates ongrowth and arsenic accumulation in Plantago lanceolata L. Environ Pollut,168:121~130
Or owska E, Ryszka P, Jurkiewicz A, Turnau K.2005. Effectiveness of arbuscular mycorrhizal fungal(AMF) strains in colonisation of plants involved in phytostabilisation of zinc wastes. Geoderma,129(1):92~98
Or owska E, Zubek S Z, Jurkiewicz A, Szarek-ukaszewska G, Turnau K.2002. Influence of restoration onarbuscular mycorrhiza of Biscutella laevigata L.(Brassicaceae) and Plantago lanceolata L.(Plantaginaceae) from calamine spoil mounds. Mycorrhiza,12(3):153~159
Ouziad F, Hildebrandt U, Schmelzer E, Bothe H.2005. Differential gene expressions in arbuscularmycorrhizal-colonized tomato grown under heavy metal stress. J Plant Physiol,162(6):634~649
Pérez-de-Mora A, Burgos P, Madejón E, Cabrera F, Jaeckel P, Schloter M.2006. Microbial communitystructure and function in a soil contaminated by heavy metals: effects of plant growth and differentamendments. Soil Biol Biochem,38(2):327~341
Pal R, Rai J P N.2010. Phytochelatins: peptides involved in heavy metal detoxification. Appl BiochemBiotechnol,160(3):945~963
Parniske M.2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Rev Microbiol,6(10):763~775
Phillips M, Hayman D S.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
Pichardo S T, Su Y, Han F X.2012. The potential effects of arbuscular mycorrhizae (AM) on the uptake ofheavy metals by plants from contaminated soils. J Bioremed Biodeg,3:e124. doi:10.4172/2155-6199.1000e124
Pickles B J, Genney D R, Anderson I C, Alexander I J.2012. Spatial analysis of ectomycorrhizal fungireveals that root tip communities are structured by competitive interactions. Mol Ecol,21(20):5110~5123
Piechalak A, Tomaszewska B, Baralkiewicz D, Malecka A.2002. Accumulation and detoxification of leadions in legumes. Phytochemistry,60:153~162
Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E.2011. Lead uptake, toxicity, and detoxification inplants. in: Whitacre, D M. Reviews of Environmental Contamination and Toxicology. Springer NewYork:113~136
Prasas D D K, Prasas A R K.1987. Altered δ-aminolevulinic acid metabolism by lead and mercury ingerminating seedlings of Bajra (Pennisetum typhoideum). J Plant Physiol,127(3-4):241~249
Punamiya P, Datta R, Sarkar D, Barber S, Patel M, Das P.2010. Symbiotic role of Glomus mosseae inphytoextraction of lead in vetiver grass [Chrysopogon zizanioides (L.)]. J Hazard Mater,177:465~474
Purin S, Rillig M.2007. The arbuscular mycorrhizal fungal protein glomalin: Limitations, progress, and anew hypothesis for its function. Pedobiologia,51:123~130
Ramos J, Naya L, Gay M, Abián J, Becana M.2008. Functional characterization of an unusualphytochelatin synthase, LjPCS3, of Lotus japonicus. Plant Physiol,148(1):536~545
Rauser, W E.1990. Phytochelatins. Ann Rev Biochem,59:61~86
Reddy A M, Kumar S G, Jyothsnakumari G, Thimmanaik S, Sudhakar C.2005. Lead induced changes inantioxidant metabolism of horsegram (Macrotyloma uniflorum (Lam.) Verdc.) and bengalgram (Cicerarietinum L.). Chemosphere,60(1):97~104
Redecker D.2000. Specific PCR primers to identify arbuscular mycorrhizal fungi within colonized roots.Mycorrhiza,10(2):73~80
Ren Y X, Zhu X L, Fan D D, Ma P, Liang L H.2013. Inoculation of phosphate solubilizing bacteria for theimprovement of lead accumulation by Brassica juncea. Environ Technol,34(4):463~469
Repetto O, Bestel-Corre G, Dumas-Gaudot E, Berta G, Gianinazzi-Pearson V, Gianinazzi S.2003.Targeted proteomics to identify cadmium-induced protein modifications in Glomus mosseae-inoculated pea roots. New Phytol,157(3):555~567
Rillig M C.2004. Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci,84:355~362
Rillig M C, Mummey D L.2006. Mycorrhizas and soil structure. New Phytol,171(1):41~53
Rillig M C, Wright S F, Nichols K A, Schmidt W F, Torn M S.2001. Large contribution of arbuscularmycorrhizal fungi to soil carbon pools in tropical forest soils. Plant Soil,233(2):167~177
Rivera-Becerril F, Calantzis C, Turnau K, Caussanel J P, Belimov A A, Gianinazzi S, Strasser R J,Gianinazzi‐Pearson V.2002. Cadmium accumulation and buffering of cadmium-induced stress byarbuscular mycorrhiza in three Pisum sativum L. genotypes. J Exp Bot,53(371):1177~1185
Rivera-Becerril F, Van-Tuinen D, Martin-Laurent F, Metwally A, Dietz K J, Gianinazzi S, Gianinazzi-Pearson V.2005. Molecular changes in Pisum sativum L. roots during arbuscular mycorrhizabuffering of cadmium stress. Mycorrhiza,16(1):51~60
Romanowska E, Wróblewska B, Dro ak A, Siedlecka M.2006. High light intensity protectsphotosynthetic apparatus of pea plants against exposure to lead. Plant Physiol Biochem,44(5):387~394
Ronquist F, Teslenko M, van der Mark P, Ayres D L, Darling A, Hohna S, Larget B, Liu L, Suchard M A,Huelsenbeck J P.2012. MrBayes3.2: efficient Bayesian phylogenetic inference and model choiceacross a large model space. Syst Biol,61(3):539~542
Rosch C, Bothe H.2005. Improved assessment of denitrifying, N2-fixing, and total-community bacteria byterminal restriction fragment length polymorphism analysis using multiple restriction enzymes. ApplEnviron Microbiol,71(4):2026~2035
Rosendahl S.2008. Communities, populations and individuals of arbuscular mycorrhizal fungi. New Phytol,178(2):253~266
Rosier C L, Hoye A T, Rillig M C.2006. Glomalin-related soil protein: Assessment of current detectionand quantification tools. Soil Biol Biochem,38(8):2205~2211
Sahi S V, Bryant N L, Sharma N C, Singh S R.2002. Characterization of a lead hyperaccumulator shrub,Sesbania drummondii. Environ Sci Tech,36(21):4676~4680
Scarano G, Morelli E.2002. Characterization of cadmium-and lead-phytochelatin complexes formed in amarine microalga in response to metal exposure. BioMetals,15(2):145~151
Schechter S P, Bruns T D.2008. Serpentine and non-serpentine ecotypes of Collinsia sparsiflora associatewith distinct arbuscular mycorrhizal fungal assemblages. Mol Ecol,17(13):3198~3210
Schloter M, Bach H J, Metz S, Sehy U, Munch J C.2003. Influence of precision farming on the microbialcommunity structure and functions in nitrogen turnover. Agr Ecosyst Environ,98(1-3):295~304
Schneider J, de-Oliveira L M, Guilherme L R G, Sturmer S L, Soares C R F S.2012. Tropicalpteridophytes species in association with arbuscular mycorrhizal fungi in arsenic-contaminated soil.Quim Nova,35(4):709~714
Schreiber U, Schliwa U, Bilger W.1986. Continuous recording of photochemical and non-photochemicalquenching with a new type of modulation fluorometer. Photosynth Res,10:51~62
Schussler A, Gehrig H, Schwarzott D, Walker C.2001. Analysis of partial Glomales SSU rRNA genesequences: implications for primer design and phylogeny. Mycol Res,105:5~15
Seregin I V, Ivanov V B.1997. Histochemical investigation of cadmium and lead distribution in plants.Russ J Plant Physiol,44(6):791~796
Seregin I V, Ivanov V B.2001. Physiological aspects of cadmium and lead toxic effects on higher plants.Russ J Plant Physiol,48(4):523~544
Shao Y H, Zhang W X, Liu Z F, Sun Y X, Chen D M, Wu J P, Zhou L X, Xia H P, Neher D A, Fu S L.2012. Responses of soil microbial and nematode communities to aluminum toxicity in vegetated oil-shale-waste lands. Ecotoxicology,21(8):2132~2142
Sheng M, Tang M, Chen H, Yang B W, Zhang F F, Huang Y H.2009. Influence of arbuscular mycorrhizaeon the root symstem of maize plants under salt stress. Can J Microbiol,55(7):879~886
Shu W S, Ye Z H, Zhang Z Q, Lan C Y, Wong M H.2005. Natural colonization of plants on five lead/zincmine tailings in southern China. Restor Ecol,13(1):49~60
Silvestri G, Santarelli S, Aquilanti L, Beccaceci A, Osimani A, Tonucci F, Clementi F.2007. Investigationof the microbial ecology of Ciauscolo, a traditional Italian salami, by culture-dependent techniquesand PCR-DGGE. Meat Sci,77(3):413~423
Simon L, Lalonde M, Bruns T D.1992. Specific amplification of18S fungal ribosomal genes fromvesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol,58(1):291~295
Singh B K, Nunan N, Ridgway K P, McNicol J, Young J P, Daniell T J, Prosser J I, Millard P.2008.Relationship between assemblages of mycorrhizal fungi and bacteria on grass roots. EnvironMicrobiol,10(2):534~541
Singh R, Tripathi R D, Dwivedi S, Kumar A, Trivedi P K, Chakrabarty D.2010. Lead bioaccumulationpotential of an aquatic macrophyte Najas indica are related to antioxidant system. Bioresour Technol,101(9):3025~3032
Smith S E, Read D J.2008. Mycorrhizal symbiosis.3rded. Amsterdam, the Netherlands: Academic Press.
Sonjak S, Beguiristain T, Leyval C, Regvar M.2009. Temporal temperature gradient gel electrophoresis(TTGE) analysis of arbuscular mycorrhizal fungi associated with selected plants from saline and metalpolluted environments. Plant Soil,314(1-2):25~34
Srivastava P K, Vaish A, Dwivedi S, Chakrabarty D, Singh N, Tripathi R D.2011. Biological removal ofarsenic pollution by soil fungi. Sci Total Environ,409(12):2430~2442
Steinberg P D, Rillig M C.2003. Differential decomposition of arbuscular mycorrhizal fungal hyphae andglomalin. Soil Biol Biochem,35(1):191~194
Steinkellner S, Hage-Ahmed K, Garcia-Garrido J M, Illana A, Ocampo J A, Vierheilig H.2012. Acomparison of wild-type, old and modern tomato cultivars in the interaction with the arbuscularmycorrhizal fungus Glomus mosseae and the tomato pathogen Fusarium oxysporum f. sp lycopersici.Mycorrhiza,22(3):189~194
Stockinger H, Walker C, Schussler A.2009."Glomus intraradices DAOM197198", a model fungus inarbuscular mycorrhiza research, is not Glomus intraradices. New Phytol,183(4):1176~1187
Sun Q, Ye Z H, Wang X R, Wong M H.2005. Increase of glutathione in mine population of Sedum alfredii:A Zn hyperaccumulator and Pb accumulator. Phytochemistry,66(21):2549~2556
Sun Q, Ye Z H, Wang X R, Wong M H.2007. Cadmium hyperaccumulation leads to an increase ofglutathione rather than phytochelatins in the cadmium hyperaccumulator Sedum alfredii. J PlantPhysiol,164(11):1489~1498
Tamura K, Dudley J, Nei M, Kumar S.2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA)software version4.0. Mol Biol Evol,24(8):1596~1599
Tarkka M, Schrey S, Hampp R.2008. Plant associated micro-organisms. Mol Mech Plant Micro Coexis,15(1):3~51
Thuong N T, Yoneda M, Ikegami M, Takakura M.2013. Source discrimination of heavy metals insediment and water of To Lich River in Hanoi City using multivariate statistical approaches. EnvironMonit Assess, doi:10.1007/s10661-013-3155-x
Tomulescu I M, Radoviciu E M, Merca V V, Tuduce A D.2004. Effect of copper, zinc and lead and theircombinations on the germination capacity of two cereals. J Agric Sci,15:39~42
Trappe J M.1987. Phylogenetic and ecologic aspects of mycotrophy in the angiosperms from anevolutionary standpoint. In: Safir, G R (ed). Ecophysiology of VA mycorrhizal plants. Boca Rato:CRC:5~25
Turnau K, Kottke I, Oberwinkler F.1993. Element localization in mycorrhizal roots of Pteridiumaquilinum (L.) Kuhn collected from experimental plots treated with cadmium dust. New Phytol,123(2):313~324
Verbruggen N, Hermans C, Schat H.2009. Molecular mechanisms of metal hyperaccumulation in plants.New Phytol,181(4):759~776
Verma S, Dubey R S.2003. Lead toxicity induces lipid peroxidation and alters the activities of antioxidantenzymes in growing rice plants. Plant Sci,164(4):645~655
Vestergaard M, Matsumoto S, Nishikori S, Shiraki K, Hirata K, Takagi M.2008. Chelation of cadmiumions by phytochelatin synthase: Role of the cystein-rich C-terminal. Anal Sci,24:277~281
Vivas A, Barea J M, Biró B, Azcón R.2006a. Effectiveness of autochthonous bacterium and mycorrhizalfungus on Trifolium growth, symbiotic development and soil enzymatic activities in Zn contaminatedsoil. J Appl Microbiol,100(3):587~598
Vivas A, Biro B, Ruiz-Lozano J M, Barea J M, Azcón R.2006b. Two bacterial strains isolated from a Zn-polluted soil enhance plant growth and mycorrhizal efficiency under Zn-toxicity. Chemosphere,62(9):1523~1533
Vivas A, V r s I, Biró B, Campos E, Barea J M, Azcón R.2003. Symbiotic efficiency of autochthonousarbuscular mycorrhizal fungus (G. mosseae) and Brevibacillus sp. isolated from cadmium polluted soilunder increasing cadmium levels. Environ Pollut,126(2):179~189
Vodnik D, Grcma H, Macek I, van-Elteren J T, Kovacevic M.2008. The contribution of glomalin-relatedsoil protein to Pb and Zn sequestration in polluted soil. Sci Total Environ,392(1):130~136
Vogel-Miku K, Drobne D, Regvar M.2005. Zn, Cd and Pb accumulation and arbuscular mycorrhizalcolonisation of pennycress Thlaspi praecox Wulf.(Brassicaceae) from the vicinity of a lead mine andsmelter in Slovenia. Environ Pollut,133(2):233~242
Volpe V, Delláglio E, Giovannetti M, Ruberti C, Costa A, Genre A, Guether M, Bonfante P.2013. An AMinduced-MYB-family gene of Lotus japonicus (LjMAMI) affects root growth in an AM-independentmanner. Plant J,73(3):442~455
Wang F Y, Lin X G, Yin R, Wu L H.2006. Effects of arbuscular mycorrhizal inoculation on the growth ofElsholtzia splendens and Zea mays and the activities of phosphatase and urease in a multi-metal-contaminated soil under unsterilized conditions. Appl Soil Ecol,31(1):110~119
Wang X, Zhou Q X.2003. Distribution of forms for cadmium, lead, copper and zinc in soil land itsinfluences by modifier. J Agr Environ Sci,22:541~545
Wang Y P, Li Q B, Shi J Y, Lin Q, Chen X C, Wu W X, Chen Y X.2008. Assessment of microbial activityand bacterial community composition in the rhizosphere of a copper accumulator and a non-accumulator. Soil Biol Biochem,40(5):1167~1177
Wawrzyński A, Kopera E, Wawrzyńska A, Kamińska J, Bal W, Sirko A.2006. Effects of simultaneousexpression of heterologous genes involved in phytochelatin biosynthesis on thiol content and cadmiumaccumulation in tobacco plants. J Exp Bot,57(10):2173~2182
Weiersbye I M, Straker C J, Przybylowicz W J.1999. Micro-PIXE mapping of elemental distribution inarbuscular mycorrhizal roots of the grass, Cynodon dactylon, from gold and uranium mine tailings.Nucl instrum meth physic res sec B: beam interact mater and atom,158(1):335~343
Weissenhorn I, Leyval C.1995. Root colonization of maize by a Cd-sensitive and a Cd-tolerant Glomusmosseae and cadmium uptake in sand culture. Plant Soil,175(2):233~238
Weissenhorn I, Mench M, Leyval C.1995. Bioavailability of heavy metals and arbuscular mycorrhiza in asewage-sludge-amended sandy soil. Soil Biol Biochem,27(3):287~296
Wojas S, Clemens S, Hennig J, Sklodowska A, Kopera E, Schat H, Bal W, Antosiewicz D M.2008.Overexpression of phytochelatin synthase in tobacco: distinctive effects of AtPCS1and CePCS geneson plant response to cadmium. J Exp Bot,59(8):2205~2219
Wong C S C, Duzgoren-Aydin N S, Aydin A, Wong M H.2007. Evidence of excessive releases of metalsfrom primitive e-waste processing in Guiyu, China. Environmen Pollut,148(1):62~72
Wright S F, Upadhyaya A.1996. Extraction of an abundant and unusual protein from soil and comparisonwith hyphal protein of arbuscular mycorrhizal fungi. Soil Sci,161:575~585
Wright S F, Upadhyaya A.1998. A survey of soils for aggregate stability and glomalin, a glycoproteinproduced by hyphae of arbuscular mycorrhizal fungi. Plant Soil,198:97~107
Wright S F, Upadhyaya A, Buyer J S.1998. Comparison of N-linked oligosaccharides of glomalin fromarbuscular mycorrhizal fungi and soils by capillary electrophoresis. Soil Biol Biochem,30(13):1853~1857
Wu S C, Cheung K C, Luo Y M, Wong M H.2006. Effects of inoculation of plant growth-promotingrhizobacteria on metal uptake by Brassica juncea. Environ Pollut,140(1):124~135
Wulf A, Manthey K, Doll J, Perlick A M, Linke B, Bekel T, Meyer F, Franken P, Kuster H, Krajinski F.2003. Transcriptional changes in response to arbuscular mycorrhiza development in the model plantMedicago truncatula. Mol Plant Microbe Interact,16(4):306~314
Wycisk K, Kim E J, Schroeder J I, Kramer U.2004. Enhancing the first enzymatic step in the histidinebiosynthesis pathway increases the free histidine pool and nickel tolerance in Arabidopsis thaliana.FEBS Lett,578(1-2):128~134
Xiong Z T, Zhao F, Li M J.2006. Lead toxicity in Brassica pekinensis Rupr.: Effect on nitrate assimilationand growth. Environ Toxicol,21(2):147~153
Yang R Y, Zan S T, Tang J J, Chen X, Zhang Q.2010. Variation in community structure of arbuscularmycorrhizal fungi associated with a Cu tolerant plant-Elsholtzia splendens. Appl Soil Ecol,44(3):191~197
Yang Y Y, Jung J Y, Song W Y, Suh H S, Lee Y.2000. Identification of rice varieties with high toleranceor sensitivity to lead and characterization of the mechanism of tolerance. Plant Physiol,124(3):1019~1026
Yao Y, Xu G, Mou D, Wang J, Ma J.2012. Subcellular Mn compartation, anatomic and biochemicalchanges of two grape varieties in response to excess manganese. Chemosphere,89(2):150~157
Zarei M, Hempel S, Wubet T, Schafer T, Savaghebi G, Jouzani G S.2010. Molecular diversity ofarbuscular mycorrhizal fungi in relation to soil chemical properties and heavy metal contamination.Environ Pollut,158:2757~2765
Zenk M H.1996. Heavy metal detoxification in higher plants-a review. Gene,179:21~30
Zhang H H, Tang M, Chen H, Zheng C L, Niu Z C.2010. Effect of inoculation with AM fungi on leaduptake, translocation and stress alleviation of Zea mays L. seedlings planting in soil with increasinglead concentrations. Euro J Soil Biol,46(5):306~311
Zhang H Y, Xu W Z, Guo J B, He Z Y, Ma M.2005. Coordinated responses of phytochelatins andmetallothioneins to heavy metals in garlic seedlings. Plant Sci,169(6):1059~1065Zhang X H, WangY S, Lin A J.2012. Effects of arbuscular mycorrhizal colonization on the growth of upland rice(Oryzal sativa L.) in soil experimentally contaminated with Cu and Pb. J Clinic Toxicol,doi:10.4172/2161-0495.S3-003
Zhang X Y, Tang L S, Zhang G, Wu H D.2009. Heavy metal contamination in a typical mining town of aminority and mountain area, South China. Bull Environ Contam Toxicol,82(1):31~38
Zhou J M, Dang Z, Cai M F, Liu C Q.2007. Soil heavy metal pollution around the Dabaoshan mine,Guangdong province, China. Pedosphere,17(5):588~594
Zhu J Y, Zhang J X, Li Q, Han T, Xie J P, Hu Y H, Chai L Y.2013. Phylogenetic analysis of bacterialcommunity composition in sediment contaminated with multiple heavy metals from the XiangjiangRiver in China. Mar Pollut Bull, http://dx.doi.org/10.1016/j.marpolbul.2013.02.023
Zhu Y G, Christie P, Scott-Laidlaw A.2001. Uptake of Zn by arbuscular mycorrhizal white clover fromZn-contaminated soil. Chemosphere,42(2):193~199