Effects of Endo- and Ectomycorrhizal Fungi on Physiological Parameters and Heavy Metals Accumulation of Two Species from the Family Salicaceae
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Water Air Soil Pollut (2012) 223:399–410 DOI 10.1007/s11270-011-0868-8 Effects of Endo- and Ectomycorrhizal Fungi on Physiological Parameters and Heavy Metals Accumulation of Two Species from the Family Salicaceae Libor Mrnka & Michal Kuchár & Zuzana Cieslarová & Pavel Matějka & Jiřina Száková & Pavel Tlustoš & Miroslav Vosátka Received: 31 December 2010 /Accepted: 13 June 2011 /Published online: 6 July 2011 # Springer Science+Business Media B.V. 2011 Abstract There is increasing interest in poplars and inoculated separately and in combination to a soil willows due to their biomass production and phytor- substrate polluted by a mixture of heavy metals emediation potential. They host two major types of (mainly Cd, Pb, and Zn). Tree species differed in mycorrhizal fungi that can substantially modulate the their mycorrhizal affinities, with poplar being colo- physiology of their hosts. In this study, the effects of nized predominantly by Glomus intraradices and endo- and ectomycorrhizal fungi on growth, physio- willow by Hebeloma mesophaeum. H. mesophaeum logical parameters, and heavy metals accumulation increased willow height and biomass, while G. intra- were studied in a pot experiment using Salix alba L. radices decreased poplar height. The photosynthetic and Populus nigra L. The mycorrhizal fungi were rate remained unchanged, and only minor changes were observed in the relative composition of photo- synthetic pigments. Poplar photosynthetic rates and Electronic supplementary material The online version of this levels of photosynthetic pigments declined, while the article (doi:10.1007/s11270-011-0868-8) contains epicuticular waxes in leaves increased toward the end supplementary material, which is available to authorized users. of the experiment, irrespective of the inoculation. H. : : L. Mrnka M. Kuchár M. Vosátka mesophaeum strongly reduced the accumulation of Department of Mycorrhizal Symbioses, Institute of Botany, Cd and Fe in willow and poplar shoots, respectively. Academy of Sciences of the Czech Republic, Our results support the use of selected mycorrhizal Zámek 1, 252 43 Průhonice, Czech Republic strains to tune phytoremediation outcomes in their : Z. Cieslarová P. Matějka plant hosts. Department of Analytical Chemistry, Institute of Chemical Technology, Prague, Keywords Photosynthesis . Photosynthetic pigments . Technická 5, 166 28 Prague 6-Dejvice, Czech Republic Phytoremediation . Populus . Raman spectroscopy. : J. Száková P. Tlustoš Salix Department of Agroenvironmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká 129, 165 21 Prague 6-Suchdol, Czech Republic 1 Introduction L. Mrnka (*) Poplars and willows have recently been extensively Department of Mycorrhizal Symbioses, Institute of Botany, tested for phytoremediation of land contaminated by Academy of Sciences of the Czech Republic, Lesní 322, 252 43 Průhonice, Czech Republic heavy metals (HMs) (Dickinson 2006; French et al. e-mail: [email protected] 2006). Their potential resides in large biomass 400 Water Air Soil Pollut (2012) 223:399–410 production, extensive root systems, considerable Wentworth 1990). The ability of a plant host to tolerance to HMs, and high accumulation of HMs in develop dual mycorrhizae may enable the plant to the biomass (Pulford and Watson 2003). Although not adapt to a wider range of edaphic or climatic without risks, the contaminated biomass can putative- conditions compared with exclusive mycorrhizal ly be used for energetic purposes (Keller et al. 2005). hosts. A dual mycorrhizal plant may also benefit The fast-growing clones of poplars and willows differ from different abilities provided by the distinct in transport and accumulation of particular HMs, groups of fungi of both mycorrhizal types (van der production of leaves/wood biomass, root architecture, Heijden 2001). interaction with soil microorganisms, and other It was hypothesized that the efficiency of phytoex- parameters (Castiglione et al. 2009; Negri et al. traction of HMs by willows can be increased through 2003; Tlustoš et al. 2007). All of the abovementioned growth promotion caused by EM fungi (Baum et al. differences have impacts on the final outcome of the 2006). Similarly, the potential of AM fungi to enhance phytoremediation process, and careful selection of phytoremediation by poplars was underscored by appropriate tree species/clones seems to be a prereq- Lingua et al. (2008). Yet, the effects of mycorrhizal uisite for any field-based phytoremediation attempts fungi are strongly species and strain dependent, and (Pulford and Watson 2003). both enhancement and attenuation of HMs accumu- Widespread aspirations to decrease the use of lation in plants due to mycorrhizal fungi have been inorganic fertilizers and pursue sustainable and reported (Baum et al. 2006; Leyval et al. 1997). Thus, environmentally friendly technologies provide strong when introducing mycorrhizal fungi by inoculation, incentives to optimize the phytoremediation process, the selection of optimal fungal strain–plant clone including its below-ground aspects. Adjusting con- combinations is necessary (Baum et al. 2006; Sudová sortia of soil microorganisms seems to be one et al. 2008). Even with pre-selection, the uptake of conceivable method (Zimmer et al. 2009). Among HMs by mycorrhizal plants is modulated by environ- soil microorganisms, mycorrhizal fungi are a logical mental factors such as the level of soil contamination choice, as they consume substantial amounts of plant- (Audet and Charest 2007). fixed carbon and provide plants with essential Despite growing knowledge of molecular mecha- nutrients (Smith and Read 1997). Mycorrhizal fungi nisms driving plant and fungal tolerance to HMs have also been repeatedly shown to increase plant (Bellion et al. 2006; Schützendübel and Polle 2002), tolerance to various abiotic and biotic stresses, there are numerous gaps in our understanding and including HMs (Adriaensen et al. 2006; Cicatelli et ability to practically use these processes. Moreover, al. 2010). A variety of mechanisms have been information about impacts of interactions of endo- proposed to explain the observed enhancement of and ectomycorrhizal fungi on dual mycorrhizal plants plant tolerance to HMs conferred by mycorrhizal that are stressed by HMs is missing. The aim of the fungi, including enhanced HM chelation, adsorption, present paper was to test the impacts of arbuscular intracellular detoxification, and alteration of plant– and ectomycorrhizal fungi (both separately and in host transcriptomic responses (Jentschke and Godbold combination) on basic physiological processes and 2000; Leyval et al. 1997). The trees of the family heavy metals transport of Populus nigra L. and Salix Salicaceae, including poplars and willows, are able to alba L. These species play important roles in form so-called dual mycorrhizae (i.e., to simulta- riparian forests (Schnitzler 1997), where dual my- neously associate with arbuscular mycorrhizal (AM) corrhizal hosts generally dominate. Two generalist and ectomycorrhizal (EM) fungi) (Vozzo and Hacskaylo ectomycorrhizal species (Hebeloma mesophaeum 1974;Chilversetal.1987). The extent of particular (Pers.) Quél. and Paxillus involutus (Batsch) Fr.) plant clone colonization by fungi of either mycorrhizal and two arbuscular mycorrhizal species (Glomus type depends on both the clone genotype and on intraradices N.C. Schenck & G.S. Sm and Glomus environmental factors, with the latter being more claroideum N.C. Schenck & G.S. Sm.) were select- important (Gehring et al. 2006; Khasa et al. 2002). ed. We hypothesized that growth, physiological Ontogenic development should also not be neglected, parameters, and HMs accumulation would be affect- as shifts between the mycorrhizal types were frequent- ed in different ways depending on the tree species ly observed in aging poplar seedlings (Lodge and and fungal types used. Water Air Soil Pollut (2012) 223:399–410 401 2 Material and Methods ula stand in the Czech Republic. We expected that PH5 would exhibit a higher tolerance to HMs 2.1 Experimental Setup: Plant and Fungal Material compared to BEG96 and wanted to test whether the tolerance would be conferred to the host plant A pot experiment was established using soil sampled (Sudová et al. 2008). at multiple heavy metal-polluted site near Příbram The EM fungal inoculum consisted of a mixture of City, Czech Republic. Basic soil parameters were as mycelium grown for 2 to 3 months simultaneously in follows: silt loam kambisol Corg 2.4%, N 0.3%, K a non-aerated liquid PDA medium and an aerated 9576 ppm, Ca 17,721 ppm, Mg 354 ppm, pH (H2O) perlite-based MMN medium (ratio 1:2). The AM 6.5, pH (KCl) 5.7 with total/exchangeable concen- fungal inoculum consisted of root fragments of trations of HMs (in parts per million: Cd 10/3.5, Pb colonized maize (4 months), extra-radical mycelium, 2,172/734, Zn 318/28). The soil substrate was sieved and spores. All of the treatments received the same through a 2-mm sieve and gamma-sterilized (25 kGy). dose of both AM inoculum (10 mL) and EM Filtered eluate of uncontaminated kambisol (1/10 v/v inoculum (20 mL). In single-strain treatments, irrele- with distilled water) was added to the soil 2 weeks vant inoculum was autoclaved prior to use. In control prior to commencing the experiment to restore treatments, both inocula were autoclaved. This ap- bacterial populations. proach ensured that all experimental treatments The experiment had a two-factorial