iForest - Biogeosciences and Forestry


Arbuscular mycorrhizal fungi as a tool to ameliorate the phytoremediation potential of poplar: biochemical and molecular aspects

Angela Cicatelli (1), Patrizia Torrigiani (2), Valeria Todeschini (3), Stefania Biondi (4)   , Stefano Castiglione (1), Guido Lingua (3)

iForest - Biogeosciences and Forestry, Volume 7, Issue 5, Pages 333-341 (2014)
doi: https://doi.org/10.3832/ifor1045-007
Published: Apr 17, 2014 - Copyright © 2014 SISEF

Review Papers

Poplar is a suitable species for phytoremediation, able to tolerate high concentrations of heavy metals (HMs). Arbuscular mycorrhizal fungi (AMF) form symbiotic associations with the roots of most land plants; they improve nutrient uptake and enhance phytoextraction of HMs while alleviating stress in the host plant. This review summarizes previous results from field and greenhouse studies conducted by us and dealing with this topic. In a field trial on a highly Zn- and Cu-contaminated site, differences in plant survival and growth were observed among 168 clones originating from natural populations of Populus alba L. and Populus nigra L. from northern Italy. After two and a half years from planting, the density, activity and metabolic versatility of the culturable fraction of the soil bacteria in the HM-polluted field was higher in the soil close to where larger poplar plants were growing, in spite of comparable HM concentrations recorded in these soils. One well-performing clone of P. alba (AL35), which accumulated a higher concentration of both metals and had high foliar polyamine (PA) levels, was used for further investigation. In a greenhouse study, AL35 cuttings pre-inoculated with AMF (Glomus mosseae or Glomus intraradices) and then transferred to pots containing soil, collected from the HM-polluted site, displayed growth comparable to that of controls grown on unpolluted soil, in spite of higher Cu and Zn accumulation. Such plants also showed an overall up-regulation of metallothionein (MT) and PA biosynthetic genes, together with increased PA levels. A genome-wide transcriptomic (cDNA-AFLP) analysis allowed the identification of a number of genes, mostly belonging to stress-related functional categories of defense and secondary metabolism, that were differentially regulated in mycorrhizal vs. non mycorrhizal plants. A proteomic analysis revealed that, depending on sampling time, changes in protein profiles were differentially affected by AMF and/or HMs. It is concluded that soil-borne microorganisms affect plant performance on HM-polluted soil. In particular, mycorrhizal plants exhibited increased capacity for phytostabilization of HMs, together with improved growth. Their greater stress tolerance may derive from the protective role of PAs, and from the strong modulation in the expression profiles of stress-related genes and proteins.


Arbuscular Mycorrhizae, Copper, Phytoremediation, Poplar, Proteome, Soil Bacteria, Transcriptome, Zinc

Authors’ address

Angela Cicatelli
Stefano Castiglione
Dipartimento di Chimica e Biologia, Università di Salerno, Fisciano (SA - Italy)
Patrizia Torrigiani
Dipartimento di Scienze Agrarie, Università di Bologna, Bologna (Italy)
Valeria Todeschini
Guido Lingua
Dipartimento di Scienze e Innovazione Tecnologica, Università del Piemonte Orientale, Alessandria (Italy)
Stefania Biondi
Dipartimento di Scienze Biologiche, Geologiche e Ambientali, Università di Bologna, Bologna (Italy)

Corresponding author

Stefania Biondi


Cicatelli A, Torrigiani P, Todeschini V, Biondi S, Castiglione S, Lingua G (2014). Arbuscular mycorrhizal fungi as a tool to ameliorate the phytoremediation potential of poplar: biochemical and molecular aspects. iForest 7: 333-341. - doi: 10.3832/ifor1045-007

Academic Editor

Alberto Santini

Paper history

Received: May 28, 2013
Accepted: Dec 31, 2013

First online: Apr 17, 2014
Publication Date: Oct 01, 2014
Publication Time: 3.57 months

Breakdown by View Type

(Waiting for server response...)

Article Usage

Total Article Views: 26858
(from publication date up to now)

Breakdown by View Type
HTML Page Views: 20268
Abstract Page Views: 1191
PDF Downloads: 4301
Citation/Reference Downloads: 25
XML Downloads: 1073

Web Metrics
Days since publication: 3692
Overall contacts: 26858
Avg. contacts per week: 50.92

Article Citations

Article citations are based on data periodically collected from the Clarivate Web of Science web site
(last update: Nov 2020)

Total number of cites (since 2014): 17
Average cites per year: 2.43


Publication Metrics

by Dimensions ©

Articles citing this article

List of the papers citing this article based on CrossRef Cited-by.

Abou-Shanab R, Ghanem K, Ghanem N, Al Kolaibe A (2008)
The role of bacteria on heavy-metal extraction and uptake by plants growing on multi-metal-contaminated soils. World Journal of Microbiology and Biotechnology 24: 253-262.
CrossRef | Gscholar
Akashi K, Nishimura N, Ishida Y, Yokota A (2004)
Potent hydroxyl radical-scavenging activity of drought-induced type-2 metallothionein in wild watermelon. Biochemical and Biophysical Research Communications 323: 72-78.
CrossRef | Gscholar
Alcazar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010)
Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231: 1237-1249.
CrossRef | Gscholar
Ali NA, Bernal MP, Ater M (2004)
Tolerance and bioaccumulation of cadmium by Phragmites australis grown in the presence of elevated concentrations of cadmium, copper, and zinc. Aquatic Botany 80: 163-176.
CrossRef | Gscholar
Aloui A, Recorbet G, Robert F, Schoefs B, Bertrand M, Henry C, Gianinazzi-Pearson V, Dumas-Gaudot E, Aschi-Smit S (2011)
Arbuscular mycorrhizal symbiosis elicits shoot proteome changes that are modified during cadmium stress alleviation in Medicago truncatula. BMC Plant Biology 11: 75-82.
CrossRef | Gscholar
Aravanopoulos FA, Kim KH, Zsuffa L (1999)
Genetic diversity of superior Salix clones selected for intensive forestry plantations. Biomass and Bioenergy 16: 249-255.
CrossRef | Gscholar
Aronsson P, Perttu K (2001)
Willow vegetation filters for wastewater treatment and soil remediation combined with biomass production. Forestry Chronicle 77: 293-299.
CrossRef | Gscholar
Bagni N, Torrigiani P (1992)
Polyamines: a new class of growth substances. In: “Progress in plant growth regulation” (Karseen CM, van Loon LC, Vreugdenhil D eds). Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 264-275.
CrossRef | Gscholar
Balestrazzi A, Botti S, Zelasco S, Biondi S, Franchin C, Calligari P, Racchi M, Turchi A, Lingua G, Berta G, Carbonera D (2009)
Expression of the PsMT (A1) gene in white poplar engineered with the MAT system is associated with heavy metal tolerance and protection against 8-hydroxy-2’-deoxyguanosine mediated-DNA damage. Plant Cell Reports 28: 1179-1192.
CrossRef | Gscholar
Belimov AA, Safronova VI, Sergeyeva TA, Egorova TN, Matveyeva VA, Tsyganov VE, Borisov AY, Tikhonovich IA, Kluge C, Preisfeld A, Dietz KJ, Stepanok VV (2001)
Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Canadian Journal of Microbiology 47: 642-652.
CrossRef | Gscholar
Bois G, Piche Y, Fung MYP, Khasa DP (2005)
Mycorrhizal inoculum potentials of pure reclamation materials and revegetated tailing sands from the Canadian oil sand industry. Mycorrhiza 15: 149-158.
CrossRef | Gscholar
Borghi M, Tognetti R, Monteforti G, Sebastiani L (2007)
Responses of Populus x euramericana (P. deltoides x P. nigra) clone Adda to increasing copper concentrations. Environmental and Experimental Botany 61: 66-73.
CrossRef | Gscholar
Castiglione S, Cicatelli A, Lupi R, Patrignani G, Fossati T, Brundu G, Sabatti M, van Loo M, Lexer C (2010)
Genetic structure and introgression in riparian populations of Populus alba L. Plant Biosystems 144: 656-668.
CrossRef | Gscholar
Castiglione S, Todeschini V, Franchin C, Torrigiani P, Gastaldi D, Cicatelli A, Rinaudo C, Berta G, Biondi S, Lingua G (2009)
Clonal differences in survival capacity, copper and zinc accumulation, and correlation with leaf polyamine levels in poplar: a large-scale field trial on heavily polluted soil. Environmental Pollution 157: 2108-2117.
CrossRef | Gscholar
Castiglione S, Franchin C, Fossati T, Lingua G, Torrigiani P, Biondi S (2007)
High zinc concentrations reduce rooting capacity and alter metallothionein gene expression in white poplar (Populus alba L. cv. Villafranca). Chemosphere 67: 1117-1126.
CrossRef | Gscholar
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. Frontiers in Physiology 3: 91.
CrossRef | Gscholar
Cicatelli A, Todeschini V, Lingua G, Biondi S, Torrigiani P, Castiglione S (2014)
Epigenetic control of heavy metal stress response in mycorrhizal versus non-mycorrhizal poplar plants. Environmental Science and Pollution Research 21: 1723-1737.
CrossRef | Gscholar
Cicatelli A, Lingua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S (2010)
Arbuscular mycorrhizal fungi restore normal growth in a white poplar clone grown on heavy metal-contaminated soil, and this is associated with upregulation of foliar metallothionein and polyamine biosynthetic gene expression. Annals of Botany 106: 791-802.
CrossRef | Gscholar
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. Environmental and Experimental Botany 75: 25-35.
CrossRef | Gscholar
Clijsters H, Cuypers A, Vangronsveld J (1999)
Physiological responses to heavy metals in higher plants: defence against oxidative stress. Zeitschrift fur Naturforschung C-A Journal of Biosciences 54: 730-734.
Cobbett C, Goldsbrough P (2002)
Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology 53: 159-182.
CrossRef | Gscholar
Copetta A, Lingua G, Berta G (2006)
Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. var. Genovese. Mycorrhiza 16: 485-494.
CrossRef | Gscholar
Dabrowska G, Hrynkiewicz K, Trejgell A (2012)
Do arbuscular mycorrhizal fungi affect metallothionein Mt2 expression in Brassica napus L. roots? Acta Biologica Cracoviensia Series Botanica 54: 34-39.
Di Baccio D, Galla G, Bracci T, Andreucci A, Barcaccia G, Tognetti R, Sebastiani L (2011)
Transcriptome analyses of Populus x euramericana clone I-214 leaves exposed to excess zinc. Tree Physiology 31: 1293-1308.
CrossRef | Gscholar
Dickinson NM, Pulford ID (2005)
Cadmium phytoextraction using short-rotation coppice Salix: the evidence trail. Environment International 31: 609-613.
CrossRef | Gscholar
Dos Santos Utmazian MN, Wenzel WW (2007)
Cadmium and zinc accumulation in willow and poplar species grown on polluted soils. Journal of Plant Nutrition and Soil Science 170: 265-272.
CrossRef | Gscholar
Dos Santos Utmazian MN, Wieshammer G, Vega R, Wenzel WW (2007)
Hydroponic screening for metal resistance and accumulation of cadmium and zinc in twenty clones of willows and poplars. Environmental Pollution 148: 155-165.
CrossRef | Gscholar
Doty SL (2008)
Enhancing phytoremediation through the use of transgenics and endophytes. New Phytologist 179: 318-333.
CrossRef | Gscholar
Edreva A, Velikova V, Tsonev T (2007)
Phenylamides in plants. Russian Journal of Plant Physiology 54: 287-301.
CrossRef | Gscholar
Fossati T, Patrignani G, Zapelli I, Sabatti M, Sala F, Castiglione S (2004)
Development of molecular markers to assess the level of introgression of Populus tremula into P. alba natural populations. Plant Breeding 123: 382-385.
CrossRef | Gscholar
Franchin C, Fossati T, Pasquini E, Lingua G, Castiglione S, Torrigiani P, Biondi S (2007)
High concentrations of zinc and copper induce differential polyamine responses in micropropagated white poplar (Populus alba). Physiologia Plantarum 130: 77-90.
CrossRef | Gscholar
Frey B, Ruedt A, Widmer F (2010)
Changes in rhizosphere bacterial populations during phytoextraction of heavy metal contaminated soil with poplar. Plant Biosystems 144: 392-395.
CrossRef | Gscholar
Gamalero E, Cesaro P, Cicatelli A, Todeschini V, Musso C, Castiglione S, Fabiani A, Lingua G (2012)
Poplar clones of different sizes, grown on a heavy metal polluted site, are associated with microbial populations of varying composition. Science of the Total Environment 425: 262-270.
CrossRef | Gscholar
Gamalero E, Lingua G, Berta G, Glick BR (2009)
Beneficial role of plant growth promoting bacteria and arbuscular mycorrhizal fungi on plant responses to heavy metal stress. Canadian Journal of Microbiology 55: 501-514.
CrossRef | Gscholar
Gohre V, Paszkowski U (2006)
Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223: 1115-1122.
CrossRef | Gscholar
Groppa M, Benavides M (2008)
Polyamines and abiotic stress: recent advances. Amino Acids 34: 35-45.
CrossRef | Gscholar
Groppa MD, Tomaro ML, Benavides MP (2007)
Polyamines and heavy metal stress: the antioxidant behavior of spermine in cadmium- and copper-treated wheat leaves. Biometals 20: 185-195.
CrossRef | Gscholar
Guerrieri E, Lingua G, Digilio MC, Massa N, Berta G (2004)
Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecological Entomology 29: 753-756.
CrossRef | Gscholar
Hanfrey C, Franceschetti M, Mayer MJ, Illingworth C, Michael AJ (2002)
Abrogation of upstream open reading frame-mediated translational control of a plant S-adenosylmethionine decarboxylase results in polyamine disruption and growth perturbations. Journal of Biological Chemistry 277: 44131-44139.
CrossRef | Gscholar
Hartmann A, Lemanceau P, Prosser JI (2008)
Multitrophic interactions in the rhizosphere - rhizosphere microbiology: at the interface of many disciplines and expertises. Fems Microbiology Ecology 65: 179.
CrossRef | Gscholar
Hassinen V, Vallinkoski VM, Issakainen S, Tervahauta A, Karenlampi S, Servomaa K (2009)
Correlation of foliar MT2b expression with Cd and Zn concentrations in hybrid aspen (Populus tremula x tremuloides) grown in contaminated soil. Environmental Pollution 157: 922-930.
CrossRef | Gscholar
He CQ, Tan G, Liang X, Du W, Chen Y, Zhi G, Zhu Y (2010)
Effect of Zn-tolerant bacterial strains on growth and Zn accumulation in Orychophragmus violaceus. Applied Soil Ecology 44: 1-5.
CrossRef | Gscholar
Hohnjec N, Vieweg ME, Puhler A, Becker A, Kuster H (2005)
Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiology 137: 1283-1301.
CrossRef | Gscholar
Hua J, Lin X, Bai J, Shao Y, Yin R, Jiang Q (2010)
Effects of arbuscular mycorrhizal fungi and earthworm on nematode communities and arsenic uptake by maize in arsenic-contaminated soils. Pedosphere 20: 163-173.
CrossRef | Gscholar
Kohler A, Blaudez D, Chalot M, Martin F (2004)
Cloning and expression of multiple metallothioneins from hybrid poplar. New Phytologist 164: 83-93.
CrossRef | Gscholar
Kopponen P, Utriainen M, Lukkari K, Suntioinen S, Karenlampi L, Karenlampi S (2001)
Clonal differences in copper and zinc tolerance of birch in metal-supplemented soils. Environmental Pollution 112: 89-97.
CrossRef | Gscholar
Kuffner M, Puschenreiter M, Wieshammer G, Gorfer M, Sessitsch A (2008)
Rhizosphere bacteria affect growth and metal uptake of heavy metal accumulating willows. Plant and Soil 304: 35-44.
CrossRef | Gscholar
Kusano T, Berberich T, Tateda C, Takahashi Y (2008)
Polyamines: essential factors for growth and survival. Planta 228: 367-381.
CrossRef | Gscholar
Kuthanova A, Gemperlova L, Zelenkova S, Eder J, Machackova I, Opatrny Z, Cvikrova M (2004)
Cytological changes and alterations in polyamine contents induced by cadmium in tobacco BY-2 cells. Plant Physiology and Biochemistry 42: 149-156.
CrossRef | Gscholar
Laureysens I, Blust R, De Temmerman L, Lemmens C, Ceulemans R (2004)
Clonal variation in heavy metal accumulation and biomass production in a poplar coppice culture. I. Seasonal variation in leaf, wood and bark concentrations. Environmental Pollution 131: 485-494.
CrossRef | Gscholar
Lebeau T, Braud A, Jezequel K (2008)
Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environmental Pollution 153: 497-522.
CrossRef | Gscholar
Lei Y, Korpelainen H, Li C (2007)
Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations. Chemosphere 68: 686-694.
CrossRef | Gscholar
Lingua G, D’Agostino G, Massa N, Antosiano M, Berta G (2002)
Mycorrhiza-induced differential response to a yellows disease in tomato. Mycorrhiza 12: 191-198.
CrossRef | Gscholar
Lingua G, Bona E, Todeschini V, Cattaneo C, Marsano F, Berta G, Cavaletto M (2012)
Effects of heavy metals and arbuscular mycorrhiza on the leaf proteome of a selected poplar clone: a time course analysis. Plos One 7 (6): e38662.
CrossRef | Gscholar
Lingua G, Franchin C, Todeschini V, Castiglione S, Biondi S, Burlando B, Parravicini V, Torrigiani P, Berta G (2008)
Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environmental Pollution 153: 137-147.
CrossRef | Gscholar
Liu J, Wu L, Wei S, Xiao X, Su C, Jiang P, Song Z, Wang T, Yu Z (2007)
Effects of arbuscular mycorrhizal fungi on the growth, nutrient uptake and glycyrrhizin production of licorice (Glycyrrhiza uralensis Fisch). Plant Growth Regulation 52: 29-39.
CrossRef | Gscholar
Lovaas E (1997)
Antioxidative and metal-chelating effects of polyamines. Advances in Pharmacology 38: 119-149.
CrossRef | Gscholar
Martin Tanguy J (1997)
Conjugated polyamines and reproductive development: biochemical, molecular and physiological approaches. Physiologia Plantarum 100: 675-688.
CrossRef | Gscholar
Mrnka L, Kuchar M, Cieslarova Z, Matejka P, Szakova J, Tlustos P, Vosatka M (2012)
Effects of endo- and ectomycorrhizal fungi on physiological parameters and heavy metals accumulation of two species from the family Salicaceae. Water Air and Soil Pollution 223: 399-410.
CrossRef | Gscholar
Ouziad F, Hildebrandt U, Schmelzer E, Bothe H (2005)
Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. Journal of Plant Physiology 162: 634-649.
CrossRef | Gscholar
Pallara G, Todeschini V, Lingua G, Camussi A, Racchi ML (2013)
Transcript analysis of stress defence genes in a white poplar clone inoculated with the arbuscular mycorrhizal fungus Glomus mosseae and grown on a polluted soil. Plant Physiology and Biochemistry 63: 131-139.
CrossRef | Gscholar
Park MS, Jung SR, Lee KH, Lee MS, Do JO, Kim SB, Bae KS (2006)
Chryseobacterium soldanellicola sp. nov. and Chryseobacterium taeanense sp. nov., isolated from roots of sand-dune plants. International Journal of Systematic and Evolutionary Microbiology 56: 433-438.
CrossRef | Gscholar
Pilon-Smits E (2005)
Phytoremediation. Annual Review of Plant Biology 56: 15-39.
CrossRef | Gscholar
Piotrowska-Seget Z, Cycon M, Kozdroj J (2005)
Metal-tolerant bacteria occurring in heavily polluted soil and mine spoil. Applied Soil Ecology 28: 237-246.
CrossRef | Gscholar
Prabhavathi V, Rajam MV (2007)
Mannitol-accumulating transgenic eggplants exhibit enhanced resistance to fungal wilts. Plant Science 173: 50-54.
CrossRef | Gscholar
Punshon T, Dickinson NM (1997)
Acclimation of Salix to metal stress. New Phytologist 137: 303-314.
CrossRef | Gscholar
Quoreshi A, Khasa D (2008)
Effectiveness of mycorrhizal inoculation in the nursery on root colonization, growth, and nutrient uptake of aspen and balsam poplar. Biomass and Bioenergy 32: 381-391.
CrossRef | Gscholar
Rajkumar M, Sandhya S, Prasad M, Freitas H (2012)
Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnology Advances 30: 1562-1574.
CrossRef | Gscholar
Rivera-Becerril F, Metwally A, Martin-Laurent F, Van Tuinen D, Dietz KJ, Gianinazzi S, Gianinazzi-Pearson V (2005)
Molecular responses to cadmium in roots of Pisum sativum L. Water Air and Soil Pollution 168: 171-186.
CrossRef | Gscholar
Rodriguez R, Redman R (2008)
More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. Journal of Experimental Botany 59: 1109-1114.
CrossRef | Gscholar
Sannazzaro AI, Echeverria M, Alberto EO, Ruiz OA, Menendez AB (2007)
Modulation of polyamine balance in Lotus glaber by salinity and arbuscular mycorrhiza. Plant Physiology and Biochemistry 45: 39-46.
CrossRef | Gscholar
Schüßler A, Walker C (2010)
The Glomeromycota: a species list with new families and new genera. The Royal Botanic Garden Edinburgh, The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University, Gloucester, UK, pp. 56.
Online | Gscholar
Sebastiani L, Scebba F, Tognetti R (2004)
Heavy metal accumulation and growth responses in poplar clones Eridano (Populus deltoides x maximowiczii) and I-214 (P. x euramericana) exposed to industrial waste. Environmental and Experimental Botany 52: 79-88.
CrossRef | Gscholar
Sharma SS, Dietz KJ (2006)
The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany 57: 711-726.
CrossRef | Gscholar
Shilev SI, Ruso J, Puig A, Benlloch M, Jorrin J, Sancho E (2001)
Rhizospheric bacteria promote sunflower (Helianthus annuus L.) plant growth and tolerance to heavy metals. Minerva Biotecnologica 13: 37-39.
Smith SE, Read DJ (1997)
Mycorrhizal symbiosis (2nd edn). Academic Press, London, UK, pp. 605.
Smith SE, Facelli E, Pope S, Smith F (2010)
Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant and Soil 326: 3-20.
CrossRef | Gscholar
Smulders M, Cottrell J, Lefevre F, van der Schoot J, Arens P, Vosman B, Tabbener H, Grassi F, Fossati T, Castiglione S, Krystufek V, Fluch S, Burg K, Vornam B, Pohl A, Gebhardt K, Alba N, Agundez D, Maestro C, Notivol E, Volosyanchuk R, Pospiskova M, Bordacs S, Bovenschen J, van Dam B, Koelewijn H, Halfmaerten D, Ivens B, van Slycken J, Broeck A, V, Storme V, Boerjan W (2008)
Structure of the genetic diversity in black poplar (Populus nigra L.) populations across European river systems: consequences for conservation and restoration. Forest Ecology and Management 255: 1388-1399.
CrossRef | Gscholar
Solis-Dominguez FA, Valentin-Vargas A, Chorover J, Maier RM (2011)
Effect of arbuscular mycorrhizal fungi on plant biomass and the rhizosphere microbial community structure of mesquite grown in acidic lead/zinc mine tailings. Science of the Total Environment 409: 1009-1016.
CrossRef | Gscholar
Takacs D, Radimszky L, Nemeth T (2005)
The arbuscular mycorrhizal status of poplar clones selected for phytoremediation of soils contaminated with heavy metals. Zeitschrift fur Naturforschung CA Journal of Biosciences 60: 357-361.
Online | Gscholar
Thewys T, Witters N, Meers E, Vangronsveld J (2010)
Economic viability of phytoremediation of a cadmium contaminated agricultural area using energy maize. Part II: economics of anaerobic digestion of metal contaminated maize in Belgium. International Journal of Phytoremediation 12: 663-679.
CrossRef | Gscholar
Todeschini V, Franchin C, Castiglione S, Burlando B, Biondi S, Torrigiani P, Berta G, Lingua G (2007)
Responses to copper of two registered poplar clones inoculated or not with arbuscular mycorrhizal fungi. Caryologia 60: 146-155.
CrossRef | Gscholar
Tognetti R, Cocozza C, Marchetti M (2013)
Shaping the multifunctional tree: the use of Salicaceae in environmental restoration. iForest 6: 37-47.
CrossRef | Gscholar
Tsai CJ, Harding SA, Tschaplinski TJ, Lindroth RL, Yuan Y (2006)
Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytologist 172: 47-62.
CrossRef | Gscholar
Tseng CC, Wang JY, Yang L (2009)
Accumulation of copper, lead, and zinc by in situ plants inoculated with AM fungi in multicontaminated soil. Communications in Soil Science and Plant Analysis 40: 3367-3386.
CrossRef | Gscholar
Tuskan GA, DiFazio SP, Teichmann T (2004)
Poplar genomics is getting popular: the impact of the poplar genome project on tree research. Plant Biology 6: 2-4.
CrossRef | Gscholar
van der Lelie D, Taghavi S, Monchy S, Schwender J, Miller L, Ferrieri R, Rogers A, Wu X, Zhu W, Weyens N, Vangronsveld J, Newman L (2009)
Poplar and its bacterial endophytes: coexistence and harmony. Critical Reviews in Plant Sciences 28: 346-358.
CrossRef | Gscholar
Velikova V, Yordanov I, Edreva A (2000)
Oxidative stress and some antioxidant systems in acid rain-treated bean plants - protective role of exogenous polyamines. Plant Science 151: 59-66.
CrossRef | Gscholar
Zalesny RS, Bauer EO, Hall RB, Zalesny JA, Kunzman J, Rog CJ, Riemenschneider DE (2005)
Clonal variation in survival and growth of hybrid poplar and willow in an in situ trial on soils heavily contaminated with petroleum hydrocarbons. International Journal of Phytoremediation 7: 177-197.
CrossRef | Gscholar

This website uses cookies to ensure you get the best experience on our website. More info