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Promotion of mycorrhiza formation and growth of willows by the bacterial strain Sphingomonas sp. 23L on fly ash

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Abstract

Re-vegetation of fly ash, the principal by-product of coal fired power stations, is hampered by its unfavourable chemical and physical properties for plant growth. In the present study, we evaluated the use of inoculation with a mycorrhiza-associated bacterial strain (Sphingomonas sp. 23L) to promote mycorrhiza formation and plant growth of three willow clones (Salix spp.) on fly ash from an over-burdened dump in a pot experiment. The high pHH2O (8.7) and low nitrogen content (Nt = 0.1 g kg−1) in combination with hydrophobicity of the particle surfaces caused low plant growth. Inoculation of the willows with Sphingomonas sp. 23L improved the nitrogen uptake by plants, increased plant growth and stimulated formation of ectomycorrhizae with an autochthonous Geopora sp. strain on all three willow clones. The ectomycorrhiza formed by the Geopora sp. was morphologically and anatomically described. The inoculation significantly increased the shoot growth of two Salix viminalis clones and the root growth of a S. viminalis x caprea hybrid clone. We conclude that inoculation with mycorrhiza promoting bacterial strains might be a suitable approach to support mycorrhiza formation with autochtonous site-adapted ectomycorrhizal fungi in fly ash and thereby to improve re-vegetation of fly ash landfills with willows.

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References

  • Agerer R (1991) Characterization of ectomycorrhiza. In: Norris JR, Read DJ, Varma AK (eds) Techniques for the study of mycorrhiza. Academic, London, pp 50–51

    Google Scholar 

  • Agerer R (ed) (1987–2006) Colour atlas of ectomycorrhizae, 1st–12th edn. Einhorn, Schwäbisch Gmünd

  • Agerer R, Rambold G (1998) DEEMY, a DELTA-based information system for characterisation and determination of ectomycorrhizae. Version 1.1. Institute for Systematic Botany, Section Mycology, University of München, Munich

    Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic Local Alignment Search Tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Baar H, Horton TR, Kretzer AM, Bruns TD (1999) Mycorrhizal colonization of Pinus muricata from resistant propagules after a stand-replacing wildfire. New Phytol 143:409–418. doi:10.1046/j.1469-8137.1999.00452.x

    Article  Google Scholar 

  • Baum C, Hrynkiewicz K (2006) Clonal and seasonal shifts in communities of saprotrophic microfungi and soil enzyme activities in the mycorrhizosphere of Salix spp. J Plant Nutr Soil Sci 169:481–487. doi:10.1002/jpln.200521922

    Article  CAS  Google Scholar 

  • Baum C, Hrynkiewicz K, Leinweber P, Meissner R (2006) Heavy metal mobilization and uptake by mycorrhizal and non-mycorrhizal willows (Salix x dasyclados). J Plant Nutr Soil Sci 169:516–522. doi:10.1002/jpln.200521925

    Article  CAS  Google Scholar 

  • Bianciotto V, Andreotti S, Balestrini R, Bonfante P, Perotto S (2001) Mucoid mutants of the biocontrol strain Pseudomonas fluorescens CHA0 show increased ability in biofilm formation on mycorrhizal and nonmycorrhizal carrot roots. Mol Plant Microbe Interact 14:255–260. doi:10.1094/MPMI.2001.14.2.255

    Article  PubMed  CAS  Google Scholar 

  • de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811. doi:10.1016/j.femsre.2004.11.005

    Article  PubMed  CAS  Google Scholar 

  • Dissing H (2000) Pezizales. In: Hansen L, Knudsen H (eds) Nordic macromycetes, vol. I. Ascomycetes. Nordsvamp, Copenhagen, Denmark, pp 55–128

    Google Scholar 

  • Dunstan WA, Malajczuk N, Dell B (1998) Effects of bacteria on mycorrhizal development and growth of container grown Eucalyptus diversicolor F. Muell. Seedlings. Plant Soil 201:241–249. doi:10.1023/A:1004329626763

    Article  CAS  Google Scholar 

  • Duponnois R, Garbaye J (1991) Effect of dual inoculation of Douglas fir with the ectomycorrhizal fungus Laccaria laccata and mycorrhization helper bacteria (MHB) in two bare-root forest nurseries. Plant Soil 138:169–176. doi:10.1007/BF00012243

    Article  Google Scholar 

  • Eberhardt U, Walter L, Kottke I (1999) Molecular and morphological discrimination between Tylospora fibrillosa and Tylospora asterophora mycorrhizae. Can J Bot 77:11–21. doi:10.1139/cjb-77-1-11

    Article  CAS  Google Scholar 

  • Enkhtuya B, Pöschl M, Vosátka M (2005) Native grass facilitates mycorrhizal colonisation and P uptake of tree seedlings in tow anthropogenic substrates. Water Air Soil Pollut 166:217–236. doi:10.1007/s11270-005-7273-0

    Article  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution Int J Org Evolution 39:783–791. doi:10.2307/2408678

    Google Scholar 

  • Frey-Klett P, Pierrat JC, Garbaye J (1999) Location and survival of mycorrhiza helper Pseudomonas fluorescens during establishment of ectomycorrhizal symbiosis between Laccaria bicolor and Douglas-fir. Appl Environ Microbiol 63:139–144

    Google Scholar 

  • Fujimura KE, Smith JE, Horton TR, Weber NS, Spatafora JW (2005) Pezizalean mycorrhizas and sporocarps in ponderosa pine (Pinus ponderosa) after prescribed fires in eastern Oregon, USA. Mycorrhiza 15:79–86. doi:10.1007/s00572-004-0303-8

    Article  PubMed  CAS  Google Scholar 

  • Gagnon J (1996) Stimulation of mycorrhization and growth for containerized Jack Pine seedlings inoculated with Laccaria bicolor and Pseudomonas fluorescens. In: Azcón-Aguilar C, Barea JM (eds) Mycorrhizas in integrated systems from genes to plant development. Proceedings of the fourth European Symposium on Mycorrhizas. pp 634–637

  • Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210. doi:10.1111/j.1469-8137.1994.tb04003.x

    Article  Google Scholar 

  • Garbaye J, Bowen GD (1989) Stimulation of ectomycorrhizal infection of Pinus radiata by some microorganisms associated with the mantle of ectomycorrhizas. New Phytol 112:383–388. doi:10.1111/j.1469-8137.1989.tb00327.x

    Article  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity of basidiomycetes: application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. doi:10.1111/j.1365-294X.1993.tb00005.x

    Article  PubMed  CAS  Google Scholar 

  • Gehring CA, Theimer TC, Whitham TG, Keim P (1998) Ectomycorrhizal fungal community structure of pinyon pines growing in two environmental extremes. Ecology 79:1562–1572

    Article  Google Scholar 

  • Grogan P, Baar J, Bruns TD (2000) Below-ground ectomycorrhizal community structure in a recently burned bishop pine forest. J Ecol 88:1051–1062. doi:10.1046/j.1365-2745.2000.00511.x

    Article  Google Scholar 

  • Haug I (2002) Identification of Picea-ectomycorrhizae by comparing DNA-sequences. Mycol Prog 1:167–178. doi:10.1007/s11557-006-0016-9

    Article  Google Scholar 

  • Hrynkiewicz K, Haug I, Baum C (2008) Ectomycorrhizal community structure under willows at former ore mining sites. Eur J Soil Biol 44:37–44. doi:10.1016/j.ejsobi.2007.10.004

    Article  Google Scholar 

  • Iyer RS, Scott JA (2001) Power station fly ash—a review of value-added utilization outside of the construction industry. Resour Conserv Recycling 31:217–228. doi:10.1016/S0921-3449(00)00084-7

    Article  Google Scholar 

  • Jala S, Goyal D (2006) Fly ash as a soil ameliorant for improving crop production—a review. Bioresour Technol 97:1136–1147. doi:10.1016/j.biortech.2004.09.004

    Article  PubMed  CAS  Google Scholar 

  • Jana TK, Srivastava AK, Csery K, Aroran DK (2000) Influence of growth and environmental conditions on cell surface hydrophobicity of Pseudomonas fluorescens in non-specific adhesion. Can J Microbiol 46:28–37. doi:10.1139/cjm-46-1-28

    Article  PubMed  CAS  Google Scholar 

  • Juwarkar AA, Jambhulkar HP (2008) Restoration of fly ash dump through biological interventions. Environ Monit Assess 139:355–365. doi:10.1007/s10661-007-9842-8

    Article  PubMed  CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. doi:10.1007/BF01731581

    Article  PubMed  CAS  Google Scholar 

  • Neuschütz C, Stoltz E, Greger M (2006) Root penetration of sealing layers made of fly ash and sewage sludge. J Environ Qual 35:1260–1268. doi:10.2134/jeq2005.0229

    Article  PubMed  CAS  Google Scholar 

  • O’Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Washington, pp 225–233

    Google Scholar 

  • Oliveira RS, Castro PML, Dodd JC, Vosátka M (2005) Synergistic effect of Glomus intraradices and Frankia spp. on the growth and stress recovery of Alnus glutinosa in an alkaline anthropogenic sediment. Chemosphere 60:1462–1470. doi:10.1016/j.chemosphere.2005.01.038

    Article  PubMed  CAS  Google Scholar 

  • Petersen PM (1985) The ecology of Danish soil-inhabiting Pezizales with emphasis on edaphic conditions. Opera Bot 77:1–38

    Google Scholar 

  • Philips JM, Hayman DS (1970) Improved procedure for clearing roots and staining parasitic and vesicular-arbuscular fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Pillukat A, Agerer R (1992) Studies on ectomycorrhizae XL—researches on the host dependent variability of Russula ochroleuca ectomycorrhizae. Z Mycol 58:211–242

    Google Scholar 

  • Pritsch K, Boyle H, Munch JC, Buscot F (1997) Characterization and identification of black alder ectomycorrhizas by PCR/RFLP analyses of the rDNA internal transcribed spacer (ITS). New Phytol 137:357–369. doi:10.1046/j.1469-8137.1997.00806.x

    Article  CAS  Google Scholar 

  • Rai UN, Pandey K, Sinha S, Singh A, Saxena R, Gupta DK (2004) Revegetating fly ash landfills with Prosopis juliflora L.: impact of different amendments and Rhizobium inoculation. Environ Int 30:293–300. doi:10.1016/S0160-4120(03)00179-X

    Article  PubMed  CAS  Google Scholar 

  • Raman N, Mahadevan A (1996) Mycorrhizal research—a priority in agriculture. In: Mukerji (ed) Concepts of mycorrhizal research. Kluwer, The Netherlands, pp 41–75

    Google Scholar 

  • Rambaut A (1996) Se-Al: sequence alignment editor. Department of Zoology, University of Oxford, Oxford, UK, http://evolve.zoo.ox.ac.uk

    Google Scholar 

  • Różycki H, Kampert M, Strzelczyk E, Li CY, Perry DA (1994) Effect of different soil bacteria on mycorrhizae formation in Scott pine (Pinus sylvestris L.) in vitro studies. Fol For Polon 36:92–102

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Selvam A, Mahadevan A (2000) Reclamation of ash pond of Neyveli Lignite Corporation, Neyveli, India. Minetech 21:81–89

    Google Scholar 

  • Selvam A, Mahadevan A (2002) Distribution of mycorrhizas in an abandoned fly ash pond and mined sites of Neyveli Lignite Corporation, Tamil Nadu, India. Basic Appl Ecol 3:277–284. doi:10.1078/1439-1791-00107

    Article  Google Scholar 

  • Standing D, Baggs EM, Wattenbach M, Smith P, Killham K (2007) Meeting the challenge of scaling up processes in the plant-soil-microbe system. Biol Fertil Soils 44:245–257. doi:10.1007/s00374-007-0249-z

    Article  Google Scholar 

  • Swofford DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods) version 4b 10. Sinauer, Sunderland, MA, USA

    Google Scholar 

  • Tedersoo L, Hansen K, Perry BA, Kjøller R (2006) Molecular and morphological diversity of Pezizalean ectomycorrhiza. New Phytol 170:581–596. doi:10.1111/j.1469-8137.2006.01678.x

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL- windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. doi:10.1093/nar/25.24.4876

    Article  PubMed  CAS  Google Scholar 

  • van den Burg J (1985) Folia analysis for determination of tree nutrition saturation—a compilation of literature data, no. 1. Institute for Forestry and Urban Ecology “De Dorschkamp”, Wageningen

    Google Scholar 

  • van der Heijden EW (2000) Differential benefits of arbuscular mycorrhizal and ectomycorrhizal infection of Salix repens. Mycorrhiza 10:185–193. doi:10.1007/s005720000077

    Article  Google Scholar 

  • Vom Berg W (1998) Utilization of fly ash in Europe. In: Verma CVJ, Lal PK, Kumar V, Lal R, Krishnamurthy R (eds) Proceedings of International Conference on Fly Ash Disposal and Utilization. vol. I. Central Board of Irrigation and Power, New Delhi, India, pp 8–14

    Google Scholar 

  • Warcup JH (1990) Occurrence of ectomycorrhizal and saprophytic discomycetes after a wild fire in an eucalypt forest. Mycol Res 94:1065–1069

    Article  Google Scholar 

  • Warcup JH (1991) The fungi forming mycorrhizas on eucalypt seedlings in regeneration coupes in Tasmania. Mycol Res 95:329–332

    Article  Google Scholar 

  • White TJ, Bruns TD, Lee SB, Taylor JW (1990) Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal RNA genes. In: Innis MA, Gelfand DH, Sninsky JN, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, New York, pp 315–322

    Google Scholar 

  • Xavier LJC, Germida JJ (2003) Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biol Biochem 35:471–478. doi:10.1016/S0038-0717(03)00003-8

    Article  CAS  Google Scholar 

  • Xu X, Sourè A, Granier C, Petitprez M (1995) An improved immunolabeling method for microtubular cytoskeleton in poplar (Populus nigra L.) free nuclear endosperm. Biotech Histochem 70:252–257. doi:10.3109/10520299509108202

    Article  PubMed  CAS  Google Scholar 

  • Zimmer D, Baum C, Leinweber P, Hrynkiewicz K, Meissner R (2009) Associated bacteria increase the phytoextraction of cadmium and zinc from metal-contaminated soil by mycorrhizal willows. Int J Phytorem 11:200–213. doi:10.1080/15226510802378483

    Article  CAS  Google Scholar 

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Acknowledgements

This investigation was supported by a Marie Curie Reintegration Grant financed by the European Commission (MYCOHELPER, MERG-CT-2004-006315) and by a grant (523-B) of the University of Torun (Poland). The bacterial strain was kindly provided by Dr. W. Wrótniak (Department of Microbiology, N. Copernicus University of Torun, Poland). The two anonymous referees are gratefully acknowledged.

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  1. Department of Microbiology, N. Copernicus University, ul. Gagarina 9, 89-100, Torun, Poland

    K. Hrynkiewicz & H. Dahm

  2. Institute of Land Use, University of Rostock, Justus-von-Liebig-Weg 6, 18059, Rostock, Germany

    C. Baum

  3. Laboratory of Electron and Confocal Microscopy, Department of Cell Biology, N. Copernicus University, ul. Gagarina 9, 89-100, Torun, Poland

    J. Niedojadło

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  1. K. Hrynkiewicz
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Correspondence to K. Hrynkiewicz.

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Hrynkiewicz, K., Baum, C., Niedojadło, J. et al. Promotion of mycorrhiza formation and growth of willows by the bacterial strain Sphingomonas sp. 23L on fly ash. Biol Fertil Soils 45, 385–394 (2009). https://doi.org/10.1007/s00374-008-0346-7

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