Skip to main content
Log in

Effects of Endo- and Ectomycorrhizal Fungi on Physiological Parameters and Heavy Metals Accumulation of Two Species from the Family Salicaceae

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

There is increasing interest in poplars and willows due to their biomass production and phytoremediation potential. They host two major types of mycorrhizal fungi that can substantially modulate the physiology of their hosts. In this study, the effects of endo- and ectomycorrhizal fungi on growth, physiological parameters, and heavy metals accumulation were studied in a pot experiment using Salix alba L. and Populus nigra L. The mycorrhizal fungi were inoculated separately and in combination to a soil substrate polluted by a mixture of heavy metals (mainly Cd, Pb, and Zn). Tree species differed in their mycorrhizal affinities, with poplar being colonized predominantly by Glomus intraradices and willow by Hebeloma mesophaeum. H. mesophaeum increased willow height and biomass, while G. intraradices decreased poplar height. The photosynthetic rate remained unchanged, and only minor changes were observed in the relative composition of photosynthetic pigments. Poplar photosynthetic rates and levels of photosynthetic pigments declined, while the epicuticular waxes in leaves increased toward the end of the experiment, irrespective of the inoculation. H. mesophaeum strongly reduced the accumulation of Cd and Fe in willow and poplar shoots, respectively. Our results support the use of selected mycorrhizal strains to tune phytoremediation outcomes in their plant hosts.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adriaensen, K., Vangronsveld, J., & Colpaert, J. V. (2006). Zinc-tolerant Suillus bovinus improves growth of Zn-exposed Pinus sylvestris seedlings. Mycorrhiza, 16, 553–558.

    Article  CAS  Google Scholar 

  • Aguillon, R. L., & Garbaye, J. (1989). Some aspects of a double symbiosis with ectomycorrhizal and VAM fungi. Agriculture, Ecosystem and Environment, 29, 263–266.

    Article  Google Scholar 

  • Arriagada, C. A., Herrera, M. A., & Ocampo, J. A. (2005). Contribution of arbuscular mycorrhizal and saprobe fungi to the tolerance of Eucalyptus globulus to Pb. Water, Air, and Soil Pollution, 166, 31–47.

    Article  CAS  Google Scholar 

  • Audet, P., & Charest, Ch. (2007). Heavy metal phytoremediation from a meta-analytical perspective. Environmental Pollution, 147, 231–237.

    Article  CAS  Google Scholar 

  • Baum, Ch, & Makeschin, F. (2000). Effects of nitrogen and phosphorus fertilization on mycorrhizal formation of two poplar clones (Populus trichocarpa and P. tremula x tremuloides). Journal of Plant and Nutrition Soil Science, 163, 491–497.

    Article  CAS  Google Scholar 

  • Baum, Ch, Hrynkiewicz, K., Leinweber, P., & Meißner, R. (2006). Heavy-metal mobilization and uptake by mycorrhizal and nonmycorrhizal willows (Salix × dasyclados). Journal of Plant and Nutrition Soil Science, 169, 516–522.

    Article  CAS  Google Scholar 

  • Bellion, M., Courbot, M., Jacob, Ch, Blaudez, D., & Chalot, M. (2006). Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiology Letters, 254, 173–181.

    Article  CAS  Google Scholar 

  • Bissonnette, L., St-Arnaud, M., & Labrecque, M. (2010). Phytoextraction of heavy metals by two Salicaceae clones in symbiosis with arbuscular mycorrhizal fungi during the second year of a field trial. Plant and Soil, 332, 55–67.

    Article  CAS  Google Scholar 

  • Castiglione, S., Franchin, C., Fossati, T., Lingua, G., Torrigiani, P., & Biondi, P. (2007). High zinc concentrations reduce rooting capacity and alter metallothionein gene expression in white poplar (Populus alba L. cv. Villafranca). Chemosphere, 67, 1117–1126.

    Article  CAS  Google Scholar 

  • Castiglione, S., Todeschini, V., Franchin, C., Torrigiani, P., Gastaldi, D., Cicatelli, A., et al. (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.

    Article  CAS  Google Scholar 

  • Chilvers, G. A., Lapeyrie, F. F., & Horan, D. P. (1987). Ectomycorrhizal vs endomycorrhizal fungi within the same root system. The New Phytologist, 107, 441–448.

    Article  Google Scholar 

  • 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. doi:10.1093/aob/mcq170.

  • Di Baccio, D., Tognetti, R., Minnocci, A., & Sebastiani, L. (2009). Responses of the Populus × euramericana clone I-214 to excess zinc: Carbon assimilation, structural modifications, metal distribution and cellular localization. Environmental and Experimental Botany, 67, 153–163.

    Article  Google Scholar 

  • Dickinson, N. M. (2006). Phytoremediation of industrially-contaminated sites using trees. NATO Science Series, 68, 229–240.

    Article  Google Scholar 

  • Dos Santos Utmazian, M. N., Schweiger, P., Sommer, P. M., Gorfer, M., Strauss, J., & Wenzel, W. W. (2007). Influence of Cadophora finlandica and other microbial treatments on cadmium and zinc uptake in willows grown on polluted soil. Plant and Soil Environment, 53, 158–166.

    Google Scholar 

  • French, Ch. J., Dickinson, N. M., & Putwain, P. D. (2006). Woody biomass phytoremediation of contaminated brownfield land. Environmental Pollution, 141, 387–395.

    Article  CAS  Google Scholar 

  • Gehring, C. A., Mueller, C., & Whitham, T. G. (2006). Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods. Oecologia, 149, 158–164.

    Article  Google Scholar 

  • Giovannetti, M., & Mosse, B. (1980). An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. The New Phytologist, 84, 489–500.

    Article  Google Scholar 

  • Harley, J. L., & Harley, E. L. (1987). A check-list of mycorrhiza in the British Flora. The New Phytologist, 105(Suppl), 1–120.

    Google Scholar 

  • Hashimoto, Y., & Higuchi, R. (2003). Ectomycorrhizal and arbuscular mycorrhizal colonization of two species of floodplain willows. Mycoscience, 44, 339–343.

    Article  Google Scholar 

  • Hrynkiewicz, K., Haug, I., & Baum, Ch. (2008). Ectomycorrhizal community structure under willows at former ore mining sites. European Journal of Soil Biology, 44, 37–44.

    Article  Google Scholar 

  • Jentschke, G., & Godbold, D. L. (2000). Metal toxicity and ectomycorrhizas. Physiologia Plantarum, 109, 107–116.

    Article  CAS  Google Scholar 

  • Keller, C., Ludwig, Ch, Davoli, F., & Wochele, J. (2005). Thermal treatment of metal-enriched biomass produced from heavy metal phytoextraction. Environmental Science and Technology, 39, 3359–3367.

    Article  CAS  Google Scholar 

  • Khasa, P. D., Chakravarty, P., Robertson, A., Thomas, B. R., & Dancik, B. P. (2002). The mycorrhizal status of selected poplar clones introduced in Alberta. Biomass and Bioenergy, 22, 99–104.

    Article  Google Scholar 

  • Koske, R. E., & Gemma, J. N. (1989). A modified procedure for staining roots to detect VA mycorrhizas. Mycological Research, 92, 486–488.

    Article  Google Scholar 

  • Krpata, D., Peinter, U., Langer, I., Fitz, W. J., & Schweiger, P. (2008). Ectomycorrhizal communities associated with Populus tremula growing on a heavy metal contaminated site. Mycological Research, 112, 1069–1079.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Li, H., Smith, F. A., Dickson, S., Holloway, R. E., & Smith, S. E. (2008). Plant growth depressions in arbuscular mycorrhizal symbioses: not just caused by carbon drain? The New Phytologist, 178, 852–862.

    Article  Google Scholar 

  • Lichtenthaler, H. K. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350–382.

    Article  CAS  Google Scholar 

  • Lingua, G., Franchin, C., Todeschini, V., Castiglione, S., Biondi, S., Burlando, B., et al. (2008). Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environmental Pollution, 153, 137–147.

    Article  CAS  Google Scholar 

  • Lodge, D. J. (1989). The influence of soil moisture and flooding on formation of VA-endo- and ectomycorrhizae in Populus and Salix. Plant and Soil, 117, 243–253.

    Article  Google Scholar 

  • Lodge, D. J., & Wentworth, T. R. (1990). Negative associations among VA-mycorrhizal fungi and some ectomycorrhizal fungi inhabiting the same root system. Oikos, 57, 347–356.

    Article  Google Scholar 

  • Lukac, M., Calfapietra, C., & Godbold, D. L. (2003). Production, turnover and mycorrhizal colonization of root systems of three Populus species grown under elevated CO2 (POPFACE). Global Change Biology, 9, 838–848.

    Article  Google Scholar 

  • Lunáčková, L., Masarovičová, E., Kráľová, K., & Streško, V. (2003). Response of fast growing woody plants from family Salicaceae to cadmium treatment. Bulletin of Environmental Contamination and Toxicology, 70, 576–585.

    Article  Google Scholar 

  • Matějka, P., Plešerová, L., Budínová, G., Havířová, K., Mulet, X., Skácel, F., et al. (2001). Vibrational biospectroscopy: what can we say about the surface wax layer of Norway spruce needles? Journal of Molecular Structure, 565–566, 305–310.

    Article  Google Scholar 

  • Negri, M. C., Gatliff, E. G., Quinn, J. J., & Hinchman, R. R. (2003). Root development and rooting at depths. In S. C. McCutcheon & J. L. Schnoor (Eds.), Phytoremediation transformation and control of contaminants (pp. 233–262). Hoboken: Wiley.

    Google Scholar 

  • Neville, J., Tessier, J. L., Morrison, I., Scarratt, J., Canning, B., & Klironomos, J. N. (2002). Soil depth distribution of ecto- and arbuscular mycorrhizal fungi associated with Populus tremuloides within a 3-year-old boreal forest clear-cut. Applied Soil Ecology, 19, 209–216.

    Article  Google Scholar 

  • Parádi, I., & Baar, J. (2006). Mycorrhizal fungal diversity in willow forests of different age along the river Waal, The Netherlands. Forest Ecology and Management, 237, 366–372.

    Article  Google Scholar 

  • Pulford, I. D., & Watson, C. (2003). Phytoremediation of heavy metal-contaminated land by trees-review. Environment International, 29, 529–540.

    Article  CAS  Google Scholar 

  • Regvar M., Likar M., Piltaver A., Kugonič N., & Smith J. E. (2010) Fungal community structure under goat willows (Salix caprea L.) growing at metal polluted site: the potential of screening in a model of phytostabilisation study. Plant and Soil, 330, 345–356.

    Google Scholar 

  • Schnitzler, A. (1997). River dynamics as a forest process: interaction between fluvial systems and alluvial forests in large European river plains. The Botanical Review, 63, 40–64.

    Article  Google Scholar 

  • Schützendübel, A., & Polle, A. (2002). Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. Journal of Experimental Botany, 53, 1351–1365.

    Article  Google Scholar 

  • Sell, J., Kayser, A., Schulin, R., & Brunner, I. (2005). Contribution of ectomycorrhizal fungi to cadmium uptake of poplars and willows from a heavily polluted soil. Plant and Soil, 277, 245–253.

    Article  CAS  Google Scholar 

  • Smith, S. E., & Read, D. J. (1997). Mycorrhizal symbiosis (2nd ed.). London, UK: Academic Press Ltd.

    Google Scholar 

  • Sudová, R., Doubková, P., & Vosátka, M. (2008). Mycorrhizal association of Agrostis capillaris and Glomus intraradices under heavy metal stress: combination of plant clones and fungal isolates from contaminated and uncontaminated substrates. Applied Soil Ecology, 40, 19–29.

    Article  Google Scholar 

  • Tlustoš, P., Száková, J., Vysloužilová, M., Pavlíková, D., Weger, J., & Javorská, H. (2007). Variation in the uptake of arsenic, cadmium, lead, and zinc by different species of willows Salix spp. grown in contaminated soils. Central European Journal of Biology, 2, 254–275.

    Article  Google Scholar 

  • van der Heijden, E. W. (2001). Differential benefits of arbuscular mycorrhizal and ectomycorrhizal infection of Salix repens. Mycorrhiza, 10, 185–193.

    Article  Google Scholar 

  • van der Heijden, E. W., & Vosátka, M. (1999). Mycorrhizal associations of Salix repens L. communities in succession of dune ecosystems. II. Mycorrhizal dynamics and interactions of ectomycorrhizal and arbuscular mycorrhizal fungi. Canadian Journal of Botany, 77, 1833–1841.

    Article  Google Scholar 

  • Vozzo, J. A., & Hacskaylo, E. (1974). Endo- and ectomycorrhizal associations in five Populus species. Bulletin of the Torrey Botanical Club, 101, 182–186.

    Article  Google Scholar 

  • Zimmer, D., Baum, Ch, Leinweber, P., Hrynkiewicz, K., & Meissner, R. (2009). Associated bacteria increase the phytoextraction of cadmium and zinc from metal-contaminated soil by mycorrhizal willows. International Journal of Phytoremediation, 11, 200–213.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We greatly acknowledge the support of the research by a grant from Norway through the Norwegian Financial Mechanism (project no. CZ0092), by the Ministry of Education, Youth and Sports of the Czech Republic (MSM 6046137307), and by the Academy of Sciences of the Czech Republic (grant AV0Z60050516). We also thank Dr. Radka Sudová for the selection of the AM strains, Mgr. Pavla Doubková for the preparation of the AM inocula, and Dr. Andrea Polle for kindly providing us the isolate P. involutus Maj.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Libor Mrnka.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Fig. S1

The x-loadings for principal component 1 (PC1) and 2 (PC2) of FT-Raman spectra (JPEG 62 kb)

High-resolution image (TIFF 4073 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mrnka, L., Kuchár, M., Cieslarová, Z. et al. Effects of Endo- and Ectomycorrhizal Fungi on Physiological Parameters and Heavy Metals Accumulation of Two Species from the Family Salicaceae. Water Air Soil Pollut 223, 399–410 (2012). https://doi.org/10.1007/s11270-011-0868-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11270-011-0868-8

Keywords

Navigation