蒙自桤木在云南重金属矿区植物修复中的应用价值评估
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摘要
利用超积累植物提取土壤中重金属的植物修复技术是极具价值的重金属污染治理技术之一。菌根能够促进植物对氮、磷、以及其它营养物质和水份的吸收,从而增强植物抵抗环境压力的能力。因此,利用植物内生真菌与宿主植物的协同作用提高修复效率是一种极具潜力的修复方案。
蒙自桤木(Alnus nepalensis)属于桦木科(Betulaceae)桤木属(Alnus),是一种生长迅速,常生长在被侵蚀的、裸露的土壤和岩石中,在喜马拉雅山脉以东常见的乡土树种。已有研究报道桤木属植物具有一定的重金属积累能力,此外,桤木属植物能够与深色有隔内生真菌(Dark Septate Endophytes, DSE)、丛枝菌根真菌(Arbuscular Mycorrhizal Fungi, AMF)、外生菌根真菌(Ectomycorrhizal Fungi, EMF)联合形成菌根,并能与弗兰克氏菌(Frankia)形成根瘤固氮。深色有隔内生真菌(DSE)是一类定殖于植物根部的小型真菌,它们广泛分布于各种生态系统中,特别是在受胁迫的环境中,是一类生态学功能尚不清楚的内生真菌。
本论文以云南募乃铅锌矿区为研究对象,对矿区内自然生长的蒙自桤木地上部分、地下部分对锌、铅、镉的吸收积累情况,及其根内DSE定殖情况进行了调查；从植物根部分离得到了一批DSE菌株,并对这些菌株进行了分子生物学的初步鉴定。探讨了纯培养条件下,这些菌株对重金属Cd2+的抗(耐)性,并对抗性菌株进行了EC5o(半效应浓度)值的测定,得到了以下的主要结果和结论：
1.用碱解离-酸性品红染色法对云南普洱市,澜沧县募乃铅锌矿区的五个样地48株蒙自桤木根内DSE和AMF定殖情况进行了调查,并对五个样地土壤中的锌、铅、镉含量进行了测定。结果发现,样地P1、P2、P3锌、铅、镉含量严重超出国家三级标准,属于重度污染区域；样地P4和P5锌、铅未超标,而镉超出国家标准,属于轻度污染区域。在所调查的蒙自桤木根内均发现DSE和AMF定殖,并形成典型的微菌核和AM结构。五个样地DSE定殖率从26.11%到35.51%,属于中度定殖,并且DSE定殖率随着土壤重金属浓度的增加而呈现出先增加后降低的趋势；AMF定殖率从20.22%到29.20%,也属于中度定殖,但是随着土壤重金属浓度的增加AMF定殖率没有明显趋势。
2.从募乃铅锌矿区五个样地的蒙自桤木根内分离得到153株深色真菌,样地P1P2、P3、P4、P5的分离比率分别为3.5：1、4.4：1、3：1、2.5：1和2.75：1,并进一步对这些真菌进行了分子鉴定,其中大部分菌株属于子囊菌(包括Cladosporium、 Exophiala、Cladophialophora、Phialophora、Leptodontidium、Paraphoma)还有一些分类地位尚不明确,在己鉴定到属的菌株中,优势属为Phialophora,共有31株。
3.对153株DSE真菌进行Cd2+的抗(耐)性的初步筛选,发现分离自重金属污染较严重的样地P1、P2和P3的100株真菌普遍对Cd2+抗性较强,甚至有19株菌在Cd2+浓度为600mg/L时,仍能生长,也有2株对Cd2+较为敏感；然而来源自样地P4、P5的53株菌对Cd2+抗性较弱,其中有23株在较低Cd2+浓度下不能生长,同时也有5株在Cd2+浓度为600mg/L时仍能正常生长。进一步对镉高抗性菌株中的11株菌进行了ECso值的测定,发现这些菌株EC50值普遍在150mg/L左右,其中分离自样地P1的菌株PB43镉抗性最强,EC50值达到了234.42mg/L。
4.对自然生长于五个样地的蒙自桤木锌、铅、镉的吸收和积累特征进行了初步研究,并对其应用于植物修复重金属污染土壤进行了评估。蒙自桤木地下部分锌、铅、镉含量的范围分别是212～6285mg kg-1,41～36846mg kg-1和6-82mg kg-1,地上部分含量分别是92-263mg kg-1,24-219mg kg-1和10～59mg kg-1.蒙自桤木对Zn的生物积累因子和生物转移因子分别是从0.19到21.92和从0.34到0.79；Pb是从0.01到7.02和从0.04到1.44；Cd是从0.12到34.36和从0.04到2.06。并通过相关性分析发现蒙自桤木地下部分重金属含量与土壤重金属含量之间存在着显著的正相关(Zn R=0.94, Pb R=0.99, Cd R=0.98; P<.01).
上述研究结果表明,DSE和AMF普遍定殖于募乃铅锌矿区自然生长的蒙自桤木根系上,是蒙自桤木根系上的一个正常组分,其生物学和生态学功能值得进一步研究；从蒙自桤木根系上分离得到了153株根内生真菌,其中Phialophora属为优势属；分离自重金属严重污染区域和轻度污染区域的DSE菌株中都存在镉高抗和敏感菌株,但来自重度污染区的DSE菌株Cd2+抗性普遍高于轻度污染区的菌株；蒙自桤木有相对较高的锌、铅、镉耐受能力,并在地下部分可以积累大量的重金属,在云南省锌铅矿区土壤重金属的植物固定、植被恢复中具有较好的应用前景。
Phytoremediation which utilize hyperaccumulating plants to extract heavy metals has recently been proposed as a promising way to remove toxicants from contaminated soils. Mycorrhiza can promote absorption of plant nitrogen, phosphorus, mineral nutrients and water, thereby enhancing plant resistance to environmental stress. Therefore, the application of plant-endophyte symbiotic system is proposed to be a potential technique to improve efficiency of phytoremediation.
Alnus nepalensis, belonging to Betulaceae, is fast growing, and colonizes denuded habitats freshly exposed soils, rocky and eroded slopes, and which is a common native species in the subtropical to temperate belts of the Himalaya. And, some reports indicated that Alnus species have the ability to accumulate heavy metals. In addition, the Alnus species may form symbiotic associations with dark septate endophytes (DSE), arbuscular mycorrhizal fungi (AMF), ectomycorrhizal fungi (EMF), and Frankia (actinomyces), and have the capability of fixing nitrogen by nodules. DSE are broadly classified as conidial or sterile septate fungal endophytes and comprise a heterogeneous assemblage of fungi, which form melanised structures such as inter-and intracellular hyphae and microsclerotia in the plant roots commonly occurred in some highly stress environments.
In the present study, the accumulation capacity for Zn, Pb and Cd by Alnus nepalensis growing in a lead and zinc mining spoil heap in Munai, Lancang County, Yunnan province, southwest China was evaluated. In addition, we surveyed the colonization of DSE in plant roots, and isolated the DSE strains from the roots, also identified based on morphological and molecular analysis. The DSE strains were selected to test their tolerances to Cd2+in vitro, and the high Cd2+resistant DSE's EC50(median effect concentration) were determined. The potential application of Alnus nepalensis-DSE for phytoremediation of Zn, Pb and Cd contaminated soil was also discussed. Results of the thesis were as follows:
1. The colonization status of AMF and DSE in Alnus nepalensis naturely growing in Munai lead-zinc mine area were examined by alkaline lysising and acid fuchsin staining.The concentrations of Zn, Pb and Cd in rhizosphere soils were also examined. The results indicated that the contents of zinc, lead and cadmium, far exceeded the third class national standard in the plot1, plot2and plot3, thus the three sampled sites should be catalogued to heavily polluted areas; in plot4and plot5, zinc, lead is not exceeded, while cadmium exceeds the national soil polluted standard, thus be considered to be lightly polluted areas. DSE and AMF colonization were found in all investigated Alnus nepalensis root samples, and microsclerotia and typical AM structures were observed. Moderate colonisation levels of DSE from26.11%to35.51%in five plots were observed, and the highest level occurred in the moderately contaminated soil (P3), and decreased with higher (P1and P2) and lower (P4and P5) available metals in the soils which showed a normal distribution. AMF colonization (20.22%-29.20%) belongs to the moderate colonization too, but no any trend was found with the increase of metal concentrations in the soil.
2. In total,153strains of DSE were isolated from48plant root samples collected in the five plots. The isolated ratio was3.5:1,4.4:1,3:1,2.5:1and2.75:1in P1, P2, P3, P4and P5, respectively. And phylogenic analysis based on their sequences of ITS rDNA showed that most of the strains belong to ascomyetes, including Cladosprium, Exophiala, Cladophialophora, Phialophora, Leptodontidium, Paraphoma, and some taxonomic status is not clear. Overall, Phialophora is the dominant genera in the roots of Alnus nepalensis, and31strains come from this genus.
3. Resistance of the153DSE strains to cadmium in vitro were initially screened, and found that100strains from PI, P2and P3were more tolerance than the53strains from P4and P5. Among the tested DSE strains,24(19from P1, P2, P3;5from P4, P5) DSE strains grew well in the medium containing600mg/L Cd. In addition, the EC50(median effect concentration) values for the resistant strains of DSE to cadmium were determined. The result showed that the EC50of11strains are generally in150mg/L or so, but the strain of PB43reached234.42mg/L. Overall, Strains isolated from the heavily polluted areas are commonly higher than lightly polluted in cadmium resistance or biomass.
4. The accumulation capacity for Zn, Pb and Cd by Alnus nepalensis growing in a lead and zinc mining spoil heap in Munai was evaluated, and the potential application of Alnus nepalensis for phytoremediation was also discussed. It was found that metal concentrations of the shoots ranged from92to263mg kg-1for Zn,24to219mg kg-1for Pb,10to59mg kg-1for Cd, respectively; and in the root heavy metal varied from116to574mg kg-1for Zn,28to3550mg kg-1for Pb, and22to95mg kg-1for Cd, respectively. Bioaccumulation factors and biotransfer factors ranged from0.19to21.92and0.34to0.79for Zn,0.01to7.02and0.04to1.44for Pb, and0.12to34.36and0.04to2.06for Cd, respectively. There was significant correlation between the root and soil metal concentration (Zn R=0.94, Pb R=0.99, Cd R=0.98; P<.01). Metal concentration in the shoot showed a good correlation with the soil Zn (R=0.97; P<0.01) and Pb (R=0.85;P<0.01), but Cd.
The above results suggested that DSE and AMF colonized in all Alnus nepalensis root samples growing in lead and zinc mining spoil heap, and they could be the important components of the root system. Their biological and ecological functions deserved further studies. One hundred and fifty-three fungal strains were isoalated from the roots of A. nepalensis, among which Phialophora isolates were dominant. Both resistant and sensitive isolates were found in root samples from lightly-contaminated and heavily-contaminated plots, but fungal isolates from heavily-contaminated plots were generally more resistant. Moreover, A. nepalensis had a relatively high tolerance to Zn, Pb and Cd, and a stronger ability for absorption and accumulation of these metals in its roots. All in all, the use of A. nepalensis as a vegetation cover for the phytostabilization of land contaminated by heavy metals in Yunnan province does seem to have considerable potential.
蒙自桤木(Alnus nepalensis)属于桦木科(Betulaceae)桤木属(Alnus),是一种生长迅速,常生长在被侵蚀的、裸露的土壤和岩石中,在喜马拉雅山脉以东常见的乡土树种。已有研究报道桤木属植物具有一定的重金属积累能力,此外,桤木属植物能够与深色有隔内生真菌(Dark Septate Endophytes, DSE)、丛枝菌根真菌(Arbuscular Mycorrhizal Fungi, AMF)、外生菌根真菌(Ectomycorrhizal Fungi, EMF)联合形成菌根,并能与弗兰克氏菌(Frankia)形成根瘤固氮。深色有隔内生真菌(DSE)是一类定殖于植物根部的小型真菌,它们广泛分布于各种生态系统中,特别是在受胁迫的环境中,是一类生态学功能尚不清楚的内生真菌。
本论文以云南募乃铅锌矿区为研究对象,对矿区内自然生长的蒙自桤木地上部分、地下部分对锌、铅、镉的吸收积累情况,及其根内DSE定殖情况进行了调查；从植物根部分离得到了一批DSE菌株,并对这些菌株进行了分子生物学的初步鉴定。探讨了纯培养条件下,这些菌株对重金属Cd2+的抗(耐)性,并对抗性菌株进行了EC5o(半效应浓度)值的测定,得到了以下的主要结果和结论：
1.用碱解离-酸性品红染色法对云南普洱市,澜沧县募乃铅锌矿区的五个样地48株蒙自桤木根内DSE和AMF定殖情况进行了调查,并对五个样地土壤中的锌、铅、镉含量进行了测定。结果发现,样地P1、P2、P3锌、铅、镉含量严重超出国家三级标准,属于重度污染区域；样地P4和P5锌、铅未超标,而镉超出国家标准,属于轻度污染区域。在所调查的蒙自桤木根内均发现DSE和AMF定殖,并形成典型的微菌核和AM结构。五个样地DSE定殖率从26.11%到35.51%,属于中度定殖,并且DSE定殖率随着土壤重金属浓度的增加而呈现出先增加后降低的趋势；AMF定殖率从20.22%到29.20%,也属于中度定殖,但是随着土壤重金属浓度的增加AMF定殖率没有明显趋势。
2.从募乃铅锌矿区五个样地的蒙自桤木根内分离得到153株深色真菌,样地P1P2、P3、P4、P5的分离比率分别为3.5：1、4.4：1、3：1、2.5：1和2.75：1,并进一步对这些真菌进行了分子鉴定,其中大部分菌株属于子囊菌(包括Cladosporium、 Exophiala、Cladophialophora、Phialophora、Leptodontidium、Paraphoma)还有一些分类地位尚不明确,在己鉴定到属的菌株中,优势属为Phialophora,共有31株。
3.对153株DSE真菌进行Cd2+的抗(耐)性的初步筛选,发现分离自重金属污染较严重的样地P1、P2和P3的100株真菌普遍对Cd2+抗性较强,甚至有19株菌在Cd2+浓度为600mg/L时,仍能生长,也有2株对Cd2+较为敏感；然而来源自样地P4、P5的53株菌对Cd2+抗性较弱,其中有23株在较低Cd2+浓度下不能生长,同时也有5株在Cd2+浓度为600mg/L时仍能正常生长。进一步对镉高抗性菌株中的11株菌进行了ECso值的测定,发现这些菌株EC50值普遍在150mg/L左右,其中分离自样地P1的菌株PB43镉抗性最强,EC50值达到了234.42mg/L。
4.对自然生长于五个样地的蒙自桤木锌、铅、镉的吸收和积累特征进行了初步研究,并对其应用于植物修复重金属污染土壤进行了评估。蒙自桤木地下部分锌、铅、镉含量的范围分别是212～6285mg kg-1,41～36846mg kg-1和6-82mg kg-1,地上部分含量分别是92-263mg kg-1,24-219mg kg-1和10～59mg kg-1.蒙自桤木对Zn的生物积累因子和生物转移因子分别是从0.19到21.92和从0.34到0.79；Pb是从0.01到7.02和从0.04到1.44；Cd是从0.12到34.36和从0.04到2.06。并通过相关性分析发现蒙自桤木地下部分重金属含量与土壤重金属含量之间存在着显著的正相关(Zn R=0.94, Pb R=0.99, Cd R=0.98; P<.01).
上述研究结果表明,DSE和AMF普遍定殖于募乃铅锌矿区自然生长的蒙自桤木根系上,是蒙自桤木根系上的一个正常组分,其生物学和生态学功能值得进一步研究；从蒙自桤木根系上分离得到了153株根内生真菌,其中Phialophora属为优势属；分离自重金属严重污染区域和轻度污染区域的DSE菌株中都存在镉高抗和敏感菌株,但来自重度污染区的DSE菌株Cd2+抗性普遍高于轻度污染区的菌株；蒙自桤木有相对较高的锌、铅、镉耐受能力,并在地下部分可以积累大量的重金属,在云南省锌铅矿区土壤重金属的植物固定、植被恢复中具有较好的应用前景。
Phytoremediation which utilize hyperaccumulating plants to extract heavy metals has recently been proposed as a promising way to remove toxicants from contaminated soils. Mycorrhiza can promote absorption of plant nitrogen, phosphorus, mineral nutrients and water, thereby enhancing plant resistance to environmental stress. Therefore, the application of plant-endophyte symbiotic system is proposed to be a potential technique to improve efficiency of phytoremediation.
Alnus nepalensis, belonging to Betulaceae, is fast growing, and colonizes denuded habitats freshly exposed soils, rocky and eroded slopes, and which is a common native species in the subtropical to temperate belts of the Himalaya. And, some reports indicated that Alnus species have the ability to accumulate heavy metals. In addition, the Alnus species may form symbiotic associations with dark septate endophytes (DSE), arbuscular mycorrhizal fungi (AMF), ectomycorrhizal fungi (EMF), and Frankia (actinomyces), and have the capability of fixing nitrogen by nodules. DSE are broadly classified as conidial or sterile septate fungal endophytes and comprise a heterogeneous assemblage of fungi, which form melanised structures such as inter-and intracellular hyphae and microsclerotia in the plant roots commonly occurred in some highly stress environments.
In the present study, the accumulation capacity for Zn, Pb and Cd by Alnus nepalensis growing in a lead and zinc mining spoil heap in Munai, Lancang County, Yunnan province, southwest China was evaluated. In addition, we surveyed the colonization of DSE in plant roots, and isolated the DSE strains from the roots, also identified based on morphological and molecular analysis. The DSE strains were selected to test their tolerances to Cd2+in vitro, and the high Cd2+resistant DSE's EC50(median effect concentration) were determined. The potential application of Alnus nepalensis-DSE for phytoremediation of Zn, Pb and Cd contaminated soil was also discussed. Results of the thesis were as follows:
1. The colonization status of AMF and DSE in Alnus nepalensis naturely growing in Munai lead-zinc mine area were examined by alkaline lysising and acid fuchsin staining.The concentrations of Zn, Pb and Cd in rhizosphere soils were also examined. The results indicated that the contents of zinc, lead and cadmium, far exceeded the third class national standard in the plot1, plot2and plot3, thus the three sampled sites should be catalogued to heavily polluted areas; in plot4and plot5, zinc, lead is not exceeded, while cadmium exceeds the national soil polluted standard, thus be considered to be lightly polluted areas. DSE and AMF colonization were found in all investigated Alnus nepalensis root samples, and microsclerotia and typical AM structures were observed. Moderate colonisation levels of DSE from26.11%to35.51%in five plots were observed, and the highest level occurred in the moderately contaminated soil (P3), and decreased with higher (P1and P2) and lower (P4and P5) available metals in the soils which showed a normal distribution. AMF colonization (20.22%-29.20%) belongs to the moderate colonization too, but no any trend was found with the increase of metal concentrations in the soil.
2. In total,153strains of DSE were isolated from48plant root samples collected in the five plots. The isolated ratio was3.5:1,4.4:1,3:1,2.5:1and2.75:1in P1, P2, P3, P4and P5, respectively. And phylogenic analysis based on their sequences of ITS rDNA showed that most of the strains belong to ascomyetes, including Cladosprium, Exophiala, Cladophialophora, Phialophora, Leptodontidium, Paraphoma, and some taxonomic status is not clear. Overall, Phialophora is the dominant genera in the roots of Alnus nepalensis, and31strains come from this genus.
3. Resistance of the153DSE strains to cadmium in vitro were initially screened, and found that100strains from PI, P2and P3were more tolerance than the53strains from P4and P5. Among the tested DSE strains,24(19from P1, P2, P3;5from P4, P5) DSE strains grew well in the medium containing600mg/L Cd. In addition, the EC50(median effect concentration) values for the resistant strains of DSE to cadmium were determined. The result showed that the EC50of11strains are generally in150mg/L or so, but the strain of PB43reached234.42mg/L. Overall, Strains isolated from the heavily polluted areas are commonly higher than lightly polluted in cadmium resistance or biomass.
4. The accumulation capacity for Zn, Pb and Cd by Alnus nepalensis growing in a lead and zinc mining spoil heap in Munai was evaluated, and the potential application of Alnus nepalensis for phytoremediation was also discussed. It was found that metal concentrations of the shoots ranged from92to263mg kg-1for Zn,24to219mg kg-1for Pb,10to59mg kg-1for Cd, respectively; and in the root heavy metal varied from116to574mg kg-1for Zn,28to3550mg kg-1for Pb, and22to95mg kg-1for Cd, respectively. Bioaccumulation factors and biotransfer factors ranged from0.19to21.92and0.34to0.79for Zn,0.01to7.02and0.04to1.44for Pb, and0.12to34.36and0.04to2.06for Cd, respectively. There was significant correlation between the root and soil metal concentration (Zn R=0.94, Pb R=0.99, Cd R=0.98; P<.01). Metal concentration in the shoot showed a good correlation with the soil Zn (R=0.97; P<0.01) and Pb (R=0.85;P<0.01), but Cd.
The above results suggested that DSE and AMF colonized in all Alnus nepalensis root samples growing in lead and zinc mining spoil heap, and they could be the important components of the root system. Their biological and ecological functions deserved further studies. One hundred and fifty-three fungal strains were isoalated from the roots of A. nepalensis, among which Phialophora isolates were dominant. Both resistant and sensitive isolates were found in root samples from lightly-contaminated and heavily-contaminated plots, but fungal isolates from heavily-contaminated plots were generally more resistant. Moreover, A. nepalensis had a relatively high tolerance to Zn, Pb and Cd, and a stronger ability for absorption and accumulation of these metals in its roots. All in all, the use of A. nepalensis as a vegetation cover for the phytostabilization of land contaminated by heavy metals in Yunnan province does seem to have considerable potential.
引文
An LY, Pan YH, Wang ZB, Zhu C.2011. Heavy metal absorption status of five plant species in monoculture and intercropping. Plant Soil.345:237-245
AOAC.1984. Official methods of analysis of the association of official analytical chemists 14th ed. Washington (DC):p.344
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Baltrenas P, Cepanko V.2009. Accumulation of heavy metals in short-rotation willow. Ekologija. 55:153-163
Barrow JR, Osuna P.2002. Phosphorus solubilization and uptake by dark septate fungi in four wing salt brush, Atrip/ex canescens (Pursh). Nutt J Arid Environ.51:449-459
Becerra A, Zak MR, Horton TR, Micolini J.2005. Ectomycorrhizal and arbuscular mycorrhizal colonization of Alnus acuminate from Calilegua National Park (Argentina). Mycorrhiza.15: 525-531
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Baker AJM.1981. Accumulators and excluders strategies in the response of plants to heavy metals. J Plant Nutr.3:643-654
Baker AJM, Reeves RD, Hajar ASM.1994. Heavy metal accumulation and tolerance in British population of the metal-lophyte Thlaspi caerulescens J.& C. Presl (Brassicaceae). New Phytol. 127:61-68
Baltrenas P, Cepanko V.2009. Accumulation of heavy metals in short-rotation willow. Ekologija. 55:153-163
Barrow JR, Osuna P.2002. Phosphorus solubilization and uptake by dark septate fungi in four wing salt brush, Atrip/ex canescens (Pursh). Nutt J Arid Environ.51:449-459
Becerra A, Zak MR, Horton TR, Micolini J.2005. Ectomycorrhizal and arbuscular mycorrhizal colonization of Alnus acuminate from Calilegua National Park (Argentina). Mycorrhiza.15: 525-531
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Berch SM, Kendrick B.1982. Vesicular-arbuscular mycorrhiza of southern Ontarion ferns and fern-allies. Mycologia.74:769-776
Blaudez D, Jacob C, Turnau K.2000. Differential responses of ectomycorrhizal fungi to heavy metals in vitro. My col Res.104:1366-1371
Bledsoe C, Klein P, Bliss LC.1990. A survey of mycorrhizal plants on Truelove Lowland, Devon Island, N.W.T., Canada.'Can J Bot.68:1848-1856
Chen SL, Peng SL, Wang ZR.1997. Structural characteristics of LaoChang Ag-Pb orefield in LanCang, Yunnan. Chin JNonferr Metal.7:1-5
Chopra BK, Bhat S, Mikheenko P, Xu Z, Yang Y, Luo X, Chen H, Zwieten L, Lilley MR, Zhang R. 2007. The characteristics of rhizosphere microbes associated with plants in arsenic contaminated soils from cattle dip sites.5ci Total Environ.378:331-342
Colpaert JV, Van Assche JA.1987. Heavy metal tolerance in some ectomycorrhizalfungi. Funct Ecol.1:415-421
Conesa HM, Faz A, Arnaldos R.2006. Heavy metal accumulation and tolerance in plants from mine tailings of the semiarid Cartagena-La Union minging district (SE Spain). Sci Total Environ. 366:1-11
Ebbs SD, Kochian LV.1997. Toxicity of zinc and copper to Brassica species:implications for phytoremediation. JEnviron Qual.26:776-781
Fraga BA, Le Tacon F.1990. Interactions between a VA mycorrhizal fungus and Frankia associated with Alder (Alnus glutinosa (L) Gaertn). Symbiosis.9:247-258
Fogarty RV, Tobin JM.1996. Fungal melanins and their interactions with metals. Enzyme microb tech.19:311-317
Gaur A, Adholeya A.2004. Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci.86:528-534
Gerhardt KE, Huang XD, Glick BR, Greenberg BM.2009. Phytoremediation and rhizoremediation of organic soil contaminants:Potential and challenges. Plant Science.176:20-30
Gohre V, Paszkowski U.2006. Contribution of the arbuscular mycorrhizal symbiosis to heavy metal Phytoremediation. Plant a.223:1115-1122
Grabisu C, Hernandez-Allica J, Barrutia O, Alkorta I, Becerril JM.2002. Phytoremediation:a technology using green plants to remove contaminants from polluted areas. Rev Environ Health. 17:75-90
Haselwandter K, Read DJ.1980. Fungal associations of roots of dominant and sub-dominant plants in high-alpine vegetation systems with special reference to mycorrhiza. Oecologia.45:57-62
Hemen S.2011. Metal hyperaccumulation in plants:a review focusing on phytoremediation technology. J Environ Sci Technol.4:118-138.
Hildebrandt U, Regvar M, Bothe H.2007. Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry.68:139-146
Horton TR, Cazares E, Bruns TD.1998. Ectomycorrhiza, vesicular arbuscular and dark septate fungal colonization of bishop pine (Pinus muricata) seedlings in the first 5 months of growth after wildfire. Mycorrhiza.8:11-18
Joner EJ, Leyval C.1997. Uptake of 109Cd by roots and hyphae of a Glomus mossaelTrifolium subterraneum mycorrhiza from soil amended with high and low concentrations of cadmium. New Phytol.135:353-360
Joner EJ, Briones R, Leyval C.2000. Metal binding capacity of arbuscular mycorrhizal mycelium. Plant Soil.226:221-234.
Jumpponen A, Trappe JM.1996. Population structure of Phialocephala fortinii on a receding glacier forefront. In:Azcon Aguilar C, Barea JM, eds. Mycorrhiza in Integrated Systems. From Genes to Plant Development. Luxemburg:Commission of the European Union (Cost 8.2).128-130
Jumpponen A. Mattson KG, Trappe JM,1998b. Mycorrhizal functioning of Phialocephala fortinii: interactions with soil nitrogen and organic matter. Mycorrhiza.7:261-265
Jumpponen A, Trappe JM,1998a. Dark septate endophytes:a review of facultative biotrophic root-colonizing fungi. New Phytologist.140:295-310
Kerstinhuss D.1980. Nitrogen fixation and biomass production in clones of Alnus incana. New Phytol.85:503-51
Khan AG, Kuek C, Chaudhry TM, Khoo CS, Hayes WJ.2000. Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere.41:197-207
Khade SW, Adgoleya A.2007. Feasible bioremediation through arbuscular mycorrhizal fungi imparting heavy metal tolerance:a retrospective. Bioremediation J.1:33-43
Landberg T, Greger M.1996. Differences in uptake and tolerance to heavy metals in Salix from unpolluted and polluted areas. Appl Geochem.11:175-180
Lee DB, Nam W, Young SK, Nam HC, Sang SL.2009. Phytoremediation of heavy metal contaminated soil in a reclaimed dredging area using Alnus species. J Ecol Field Biol.32: 267-275
Leyval C, Turnau K, Haselwandter K.1997. Effect of heavy metal pollution on mycorrhizal colonization and function:physiological, ecological and applied aspects. Mycorrhiza.7: 139-153
Li AR, Guan KY.2007. Mycorrhizal and dark septate endophytic fungi of Pedicularis species from northwest of Yunnan Province, China. Mycorrhiza.17:103-109
Likar M, Regvar M.2009. Application of temporal temperature gradient gel electrophoresis for characterization of fungal endophyte communities of Salix caprea L. in a heavy metal polluted soil. Sci Total Environ.407:6179-6187
Lu RK.2000. Methods of Soil and Agricultural Chemistry Analysis. China Agricultural Scientech Press, Beijing.
Lynch JM, Moffat AJ.2005. Bioremediation-prospects for the future application of innovative applied biological research. Ann Appl Biol.146:7-221
Mandyam K, Jumpponen A.2005. Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol.53:173-189
Mandyam K, Jumpponen A.2008. Seasonal and temporal dynamics of arbuscular mycorrhizal and dark septate endophytic fungi in a tallgrass prairie ecosystem are minimally affected by nitrogen enrichment. Mycorrhiza.18:145-155
Mcgonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA.1990. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol.115:495-501
McGrath SP, Lombi E,Zhao FJ.2001. What's new about cadmium hyperaccumulation. New Phytol. 149:2-3
Menkis A, Allmer J, Vasiliauskas R, Lygis V, Stenlid J, Finlay R.2004. Ecology and molecular characterization of dark septate fungi from roots, living stems, coarse and fine woody debris. Mycol Res.108:965-973
Mertens J, Vervaeke P, De Schrijver A, Luyssaert S.2006. Metal uptake by young trees from dredged brackish sediment:limitations and possibilities for phytoextraction and phytostabilisation. Sci Total Environ.326:209-215
Michail O, Wheeler CT, Hooker JE.2009. Both the arbuscular mycorrhizal fungus Gigaspora rosea and Frankia increase root system branching and reduce root hair frequency in Alnus glutinosa. Mycorrhiza.2:117-126
Michail O, Wheeler CT, Hooker JE.2010. Both the arbuscular mycorrhizal fungus Gigaspora rosea and Frankia increase root system branching and reduce root hair frequency in Alnus glutinosa. Mycorrhiza.20:117-126
Mullen RB, Schmidt SK, Jaeger CH.1998. Nitrogen uptake during snow melt by the snow buttercup, Ranunculus adoneus. Arctic Alpine Res.30:121-125
Newsham KK, Upson R, Read DJ.2009. Mycorrhizas and dark septate endophytes in polar regions. Fungal Ecology.2:10-20
Newsham KK.2011. A meta-analysis of plant responses to dark septate root endophytes. New Phytol.190:783-793
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