Skip to main content
SpringerLink
Log in

Inoculation with a ligninolytic basidiomycete, but not root symbiotic ascomycetes, positively affects growth of highbush blueberry (Ericaceae) grown in a pine litter substrate

Ligninolytic basidiomycete enhances growth of blueberry

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Ericoid mycorrhizal (ErM) fungi and other ericaceous root symbionts do not completely degrade lignin, therefore the presence of lignin in organic residues may present a barrier to nutrient uptake by ericaceous plants. Due to specialization of ErM and saprotrophic, lignin-degrading fungi in litter decomposition and nutrient mobilization, we hypothesized that the presence of both types of fungi may exert a synergism in the proximity of plant detritus, thereby increasing the growth of plants over those grown with only one type or no added fungi.

Methods

We tested this hypothesis by introducing ascomycetous ErM or root-endophytic fungi and the saprotrophic basidiomycete Agrocybe praecox to highbush blueberry (Vaccinium corymbosum) grown in a substrate of pine litter, bark and wood chips in a container experiment, and measured plant nutrient status and growth parameters over 30-months.

Results

We detected no synergistic or antagonistic interactions between the saprotrophic basidiomycete and the root-symbiotic ascomycetes. Addition of lignin-degrading A. praecox but not ErM or endophytic symbionts positively impacted shoot growth, plant biomass, total P and N uptake from the substrate and precocity in fruit bearing despite widely acknowledged high saprotrophic abilities of the latter.

Conclusions

We propose that lignin-degrading basidiomycetes are compatible with ericoid mycorrhizal roots and asymbiotically enhance plant growth via the release of N, P, and other nutrients from lignin-rich plant residues, thereby attenuating potential nutrient competition between plants and microbes as low quality litter decomposes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allison SD, LeBauer DS, Ofrecio MR, Reyes R, Ta A-M, Tran TM (2009) Low levels of nitrogen addition stimulate decomposition by boreal forest fungi. Soil Biol Biochem 41:293–302

    Article  CAS  Google Scholar 

  • Allison SD, Weintraub MN, Gartner TB, Waldrop MP (2011) Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. In: Shukla G, Varma A (eds) Soil Enzymology. Soil Biology 22. Springer, Berlin, pp 229–243. ISBN 978-3-642-14224-6

    Google Scholar 

  • Bajwa R, Abuarghub S, Read DJ (1985) The biology of mycorrhiza in the Ericaceae. X. The utilization of proteins and the production of proteolytic enzymes by the mycorrhizal endophyte and by mycorrhizal plants. New Phytol 101:469–486

    Article  CAS  Google Scholar 

  • Bañados MP (2009) Expanding blueberry production into non-traditional production areas: Northern Chile and Argentina, Mexico and Spain. Acta Hortic 810:439–444

    Google Scholar 

  • Bending GD, Read DJ (1997) Lignin and soluble phenolic degradation by ectomycorrhizal and ericoid fungi. Mycol Res 101:1348–1354

    Article  CAS  Google Scholar 

  • Berg B, McClaugherty C (1987) Nitrogen release from litter in relation to the disappearance of lignin. Biogeochemistry 4:219–224

    Article  CAS  Google Scholar 

  • Berta G, Gianinazzi-Pearson V, Gay G, Torri G (1988) Morphogenetic effects of endomycorrhizae formation on the root system of Calluna vulgaris (L.) Hull. Symbiosis 5:33–44

    CAS  Google Scholar 

  • Bird JA, Kleber M, Torn MS (2008) 13 C and 15 N stabilization dynamics in soil organic matter fractions during needle and fine root decomposition. Org Geochem 39:465–477

    Article  CAS  Google Scholar 

  • Boberg JB, Finlay RD, Stenlid J, Lindahl BD (2010) Fungal C translocation restricts N-mineralization in heterogeneous environments. Funct Ecol 24:454–459

    Article  Google Scholar 

  • Boddy L (1993) Saprotrophic cord-forming fungi: warfare strategies and other ecological aspects. Mycol Res 97:641–655

    Article  Google Scholar 

  • Brannen P, Stanaland D, NeSmith DS (2006) Use of phosphite fungicides for control of blueberry diseases in Georgia. In: NeSmith DS (ed) Proceedings of the 10th North American Blueberry Research and Extension Workers’ Conference (pp. 129-138). University of Georgia, Tifton, USA

  • Brannen PM, Harmon P, NeSmith DS (2009) Utility of phosphonate fungicides for management of Phytophthora root rot in blueberry. Acta Hortic 810:331–340

    CAS  Google Scholar 

  • Burke RM, Cairney JWG (1998) Carbohydrate oxidases in ericoid and ectomycorrhizal fungi: a possible source of Fenton radicals during the degradation of lignocellulose. New Phytol 39:637–645

    Article  Google Scholar 

  • Cairney JWG, Burke RM (1998) Extracellular enzyme activities of the ericoid mycorrhizal endophyte Hymenoscyphus ericae (Read) Korf & Kernan: their likely roles in decomposition of dead plant tissue in soil. Plant Soil 205:181–192

    Article  CAS  Google Scholar 

  • Caporn SJM, Song W, Read DJ, Lee JA (1995) The effect of repeated nitrogen fertilization on mycorrhizal infection in heather [Calluna vulgaris (L.) Hull]. New Phytol 129:605–609

    Article  Google Scholar 

  • Demchak K (2010) Blueberries. In: Kirsten A (ed) The Mid-Atlantic Berry Guide (pp. 109-160). http://pubs.cas.psu.edu/freepubs/pdfs/AGRS097h.pdf

  • Dighton J, Thomas ED, Latter PM (1987) Interactions between tree roots, mycorrhizas, a saprotrophic fungus and the decomposition of organic substrates in a microcosm. Biol Fertil Soils 4:145–150

    Article  Google Scholar 

  • Dill I, Salnikow J, Kraepelin G (1984) Hydroxyproline-rich protein material in wood and lignin of Fagus sylvatica. Appl Environ Microbiol 48:1259–1261

    PubMed  CAS  Google Scholar 

  • Gorman NR, Starrett MC (2003a) Host range of a select isolate of the ericoid mycorrhizal fungus Hymenoscyphus ericae. HortSci 38:1163–1166

    Google Scholar 

  • Gorman NR, Starrett MC (2003b) Screening commercial peat and peat-based products for the presence of ericoid mycorrhizae. J Environ Hortic 21:30–33

    Google Scholar 

  • Gramss G, Voigt K-D, Bergman H (2005) Factors influencing water solubility and plant availability of mineral compounds in the tripartite fairy rings of Marasmius oreades (Bolt.:Fr) Fr. J Basic Microbiol 1:41–54

    Article  Google Scholar 

  • Hanson EJ, Hancock JF (1996) Managing the nutrition of highbush blueberries. Michigan State University Extension Bulletin E-2011

  • Haselwandter K, Bobleter O, Read DJ (1990) Degradation of 14 C-labelled lignin and dehydropolymer of coniferyl alcohol by ericoid and ectomycorrhizal fungi. Arch Microbiol 153:352–354

    Article  CAS  Google Scholar 

  • Hobbie JE, Hobbie EA (2006) 15 N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in arctic tundra. Ecology 87:816–822

    Article  PubMed  Google Scholar 

  • Hobbie EA, Horton TR (2007) Evidence that saprotrophic fungi mobilise carbon and mycorrhizal fungi mobilize nitrogen during litter decomposition. New Phytol 173:447–449

    Article  PubMed  CAS  Google Scholar 

  • Hobbie EA, Macko SA, Shugart HH (1999) Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia 118:353–360

    Article  Google Scholar 

  • Hofland-Zijlstra JD, Berendse F (2009) The effect of nutrient supply and light intensity on tannins and mycorrhizal colonization in Dutch heathland ecosystems. Plant Ecol 201:661–675

    Article  Google Scholar 

  • Hofmockel KS, Zak DR, Blackwood CB (2007) Does atmospheric NO -3 deposition alter the abundance and activity of ligninolytic fungi in forest soils? Ecosystems 10:1278–1286

    Article  CAS  Google Scholar 

  • Hutton BJ, Dixon KW, Sivasithamparam K, Pate JS (1997) Effect of habitat disturbance on inoculum potential of ericoid endophytes of Western Australian heaths (Epacridaceae). New Phytol 135:739–744

    Article  Google Scholar 

  • Ishida TA, Nordin A (2010) No evidence that nitrogen enrichment affect fungal communities of Vaccinium roots in two contrasting boreal forest types. Soil Biol Biochem 42:234–243

    Article  CAS  Google Scholar 

  • Jansa J, Vosátka M (2000) In vitro and post vitro inoculation of micropropagated rhododendrons with ericoid mycorrhizal fungi. Appl Soil Ecol 15:125–136

    Article  Google Scholar 

  • Johansson M (2000) The influence of ammonium nitrate on the root growth and ericoid mycorrhizal colonization of Calluna vulgaris (L.) Hull from a Danish Heathland. Oecologia 123:418–424

    Article  Google Scholar 

  • Keeler BL, Hobbie SE, Kellogg LE (2009) Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites: implications for litter and soil organic matter decomposition. Ecosystems 12:1–15

    Article  CAS  Google Scholar 

  • Kerley SJ, Read DJ (1998) The biology of mycorrhiza in the Ericaceae. XX. Plant and mycorrhizal necromass as nitrogenous substrates for the ericoid mycorrhizal fungus Hymenoscyphus ericae and its hosts. New Phytol 139:353–360

    Article  Google Scholar 

  • Kirk TK, Farrell RL (1987) Enzymatic “combustion”: the microbial degradation of lignin. Annu Rev Microbiol 41:465–505

    Article  PubMed  CAS  Google Scholar 

  • Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162

    Article  Google Scholar 

  • Korcak RF (1989) Variation in nutrient requirements of blueberries and other calcifuges. HortSci 24:573–578

    Google Scholar 

  • Kosola KR, Workmaster BA (2007) Mycorrhizal colonization of cranberry: effects of cultivar, soil type, and leaf litter composition. J Am Soc Hortic Sci 132:134–141

    CAS  Google Scholar 

  • Krewer G, Ruter J (2009) Fertilizing blueberries in pine bark beds. University of Georgia Cooperative Extension Bulletin 1291

  • Leake JR, Donnelly DP, Saunders EM, Boddy L, Read DJ (2001) Rates and quantities of carbon flux to ectomycorrhizal mycelium following 14 C pulse labeling of Pinus sylvestris seedlings: effects of litter patches and interaction with a wood-decomposing fungus. Tree Physiol 21:71–82

    Article  PubMed  CAS  Google Scholar 

  • Leatham GF, Kirk TK (1983) Regulation of ligninolytic activity by nutrient nitrogen in white rot basidiomycetes. FEMS Microbiol Lett 16:65–67

    Article  CAS  Google Scholar 

  • Lindahl B, Stenlid J, Olsson S, Finlay R (1999) Translocation of 32P between interacting mycelia of a wood-decomposing fungus and ectomycorrhizal fungi in microcosm systems. New Phytol 144:183–193

    Article  CAS  Google Scholar 

  • Lindahl B, Taylor AFS, Finlay RD (2002) Defining nutritional constraints on carbon cycling in boreal forests – towards a less ‘phycocentric’ perspective. Plant Soil 242:123–135

    Article  CAS  Google Scholar 

  • Lindahl B, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay R (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620

    Article  PubMed  CAS  Google Scholar 

  • Luo ZB, Calfapietra C, Scarascia-Mugnozza G, Liberloo M, Polle A (2008) Carbon-based secondary metabolites and internal nitrogen pools in Populus nigra under Free Air CO2 Enrichment (FACE) and nitrogen fertilisation. Plant Soil 12:45–57

    Article  Google Scholar 

  • Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonizing dark septate endophytic fungi. Stud Mycol 53:173–189

    Article  Google Scholar 

  • Mulder MM, Pureveen JBM, Boon JJ, Martínez AT (1991) An analytical pyrolysis mass spectrometric study of Eucryphia cordifolia wood decayed by white-rot and brown-rot fungi. J Anal Appl Pyrol 19:175–191

    Article  CAS  Google Scholar 

  • Osono T, Takeda H, Azuma J (2008) Carbon isotope dynamics during leaf litter decomposition with reference to lignin fractions. Ecol Res 1:51–55

    Article  Google Scholar 

  • Osono T, Hobara S, Hishinuma T, Azuma J (2011) Selective lignin decomposition and nitrogen mineralization in forest litter colonized by Clitocybe sp. Eur J Soil Biol 47:114–121

    Article  CAS  Google Scholar 

  • Pearson V, Read DJ (1973) The biology of mycorrhiza in the Ericaceae. I. The isolation of the endophyte and synthesis of mycorrhizas in aseptic culture. New Phytol 72:371–379

    Article  Google Scholar 

  • Piercey MM, Thormann MN, Currah RS (2002) Saprobic characteristics of three fungal taxa from ericalean roots and their association with the roots of Rhododendron groenlandicum and Picea mariana in culture. Mycorrhiza 12:175–180

    Article  PubMed  CAS  Google Scholar 

  • Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–390

    Article  Google Scholar 

  • Rice AV, Tsuneda A, Currah RS (2006) In vitro decomposition of Sphagnum by some microfungi resembles white rot of wood. FEMS Microbiol Ecol 56:372–382

    Article  PubMed  CAS  Google Scholar 

  • Robertson GP, Groffman PM (2007) Nitrogen transformations. In: Paul EA (ed) Soil Microbiology, Ecology & Biochemistry. Academic, Oxford, UK, pp 341–364

    Chapter  Google Scholar 

  • Scagel CF (2003) Mycorrhizal status of sand-based cranberry (Vaccinium macrocarpon) bogs in southern Oregon. Small Fruits Rev 2:31–41

    Article  Google Scholar 

  • Scagel CF (2005) Inoculation with ericoid mycorrhizal fungi alters fertilizer use of highbush blueberry cultivars. HortSci 40:786–794

    Google Scholar 

  • Schmid A, Suter F, Weibel FP, Daniel C (2009) New approaches to organic blueberry (Vaccinium corymbosum) production in alkaline field soils. Eur J Hortic Sci 74:103–111

    CAS  Google Scholar 

  • Shaw TM, Dighton J, Sanders FE (1995) Interactions between ectomycorrhizal and saprotrophic fungi on agar and in association with seedlings of lodgepole pine (Pinus contora). Mycol Res 99:159–165

    Article  Google Scholar 

  • Sinsabaugh RL, Follstad Shah JJ (2011) Ecoenzymatic stoichiometry of recalcitrant organic matter decomposition: the growth rate hypothesis in reverse. Biogeochemistry 102:31–43

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24

    Article  CAS  Google Scholar 

  • Šnajdr J, Valášková V, Merhautová V, Cajthaml T, Baldrian P (2008) Activity and spatial distribution of lignocellulose-degrading enzymes during forest soil colonization by saprotrophic basidiomycetes. Enzyme Microb Technol 43:186–192

    Article  Google Scholar 

  • Steffen KT, Hofrichter M, Hatakka A (2002) Purification and characterization of manganese peroxidases from the litter-decomposing basidiomycetes Agrocybe praecox and Stropharia coronilla. Enzyme Microb Technol 30:550–555

    Article  CAS  Google Scholar 

  • Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451

    Article  PubMed  Google Scholar 

  • Strik B (2005) Blueberry: an expanding world berry crop. Chronica Hortic 45:7–12

    Google Scholar 

  • Trehane J (2004) Blueberries, Cranberries and Other Vacciniums. Timber Press, Portland, USA

    Google Scholar 

  • Valášková V, Baldrian P (2006) Estimation of bound and free fractions of lignocellulose-degrading enzymes of wood-rotting fungi Pleurotus ostreatus, Trametes versicolor and Piptoporus betulinus. Res Microbiol 157:119–124

    Article  PubMed  Google Scholar 

  • van der Wal A, van Veen JA, Pijl AS, Summerbell RC, de Boer W (2006) Constraints on development of fungal biomass and decomposition processes during restoration of arable sandy soils. Soil Biol Biochem 38:2890–2902

    Article  Google Scholar 

  • van der Wal A, de Boer W, Smant W, van Veen JJ (2007) Initial decay of woody fragments is influenced by size, vertical position, nitrogen availability and soil origin. Plant Soil 301:189–201

    Article  Google Scholar 

  • Vohník M, Albrechtová J (2011) The co-occurrence and morphological continuum between ericoid mycorrhiza and dark septate endophytes in roots of six European Rhododendron species. Folia Geobot 46:373–386

    Article  Google Scholar 

  • Vohník M, Lukančič S, Bahor E, Regvar M, Vosátka M, Vodnik D (2003) Inoculation of Rhododendron cv. Belle-Heller with two strains of Phialocephala fortinii in two different substrates. Folia Geobot 38:191–200

    Article  Google Scholar 

  • Vohník M, Albrechtová J, Vosátka M (2005) The inoculation with Oidiodendron maius and Phialocephala fortinii alters phosphorus and nitrogen uptake, foliar C:N ratio and root biomass distribution in Rhododendron cv. Azurro. Symbiosis 40:87–96

    Google Scholar 

  • Vohník M, Albrechtová J, Vosátka M (2008) The application of inocula based on ericoid mycorrhizal, DSE and saprotrophic fungi in conventional, semi-conventional, semi-organic and organic cultivation of highbush blueberries. In: Feldmann F, Kapulnik Y, Baar J (eds) Mycorrhiza Works. Phytomedizinische Gesellschaft, Braunschweig, Germany, pp 173–185. ISBN 978-3-941261-01-3

    Google Scholar 

  • Vosátka M, Gryndler M, Jansa J, Vohník M (2000) Post vitro mycorrhization and bacterization of micropropagated strawberry, potato and Azalea. Acta Hortic 530:313–324

    Google Scholar 

  • Waldrop MP, Zak DR (2006) Response of oxidative enzyme activities to nitrogen deposition affects soil concentrations of dissolved organic carbon. Ecosystems 9:921–933

    Article  CAS  Google Scholar 

  • Yang WQ, Goulart BL, Demchak K (1996) The effect of aluminum and media on the growth of mycorrhizal and nonmycorrhizal highbush blueberry plantlets. Plant Soil 183:301–308

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study is a part of the research project AV0Z60050516 of the Institute of Botany ASCR and was sponsored by Ministry of Education, Youth and Sports of the Czech Republic (OE08019 and OC09057). It would not have been possible to write this paper without support from the Grant Agency of the Czech Republic (GACR 206/09/P340). Authors wish to thank Atlantic Blue S.A. (Matalascañas, Spain) for the plant material and excellent hospitality and Petr Kolomý, Aleš Látr (Symbio-m s.r.o., Lanškroun, Czech Republic) and Andrea Kodoňová for technical help. J.J.S. is grateful for a scholarship from the J.W. Fulbright Commission. Valuable comments of two anonymous reviewers and Thomas W. Kuyper (editor) are greatly appreciated.

Author information

Authors and Affiliations

  1. Department of Mycorrhizal Symbioses, Institute of Botany ASCR, Lesni 322, CZ-252 43, Průhonice, Czech Republic

    Martin Vohník, Jesse J. Sadowsky, Tereza Lukešová, Jana Albrechtová & Miroslav Vosátka

  2. Department of Experimental Plant Biology, Faculty of Science, Charles University in Prague, Viničná 5, CZ-128 44, Prague, Czech Republic

    Martin Vohník, Tereza Lukešová & Jana Albrechtová

  3. Symbiom s.r.o., Sázava 170, CZ-563 01, Lanškroun, Czech Republic

    Miroslav Vosátka

Authors
  1. Martin Vohník
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jesse J. Sadowsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tereza Lukešová
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jana Albrechtová
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miroslav Vosátka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Vohník.

Additional information

Responsible Editor: Thom W. Kuyper.

Martin Vohník and Jesse J. Sadowsky contributed equally to this work

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vohník, M., Sadowsky, J.J., Lukešová, T. et al. Inoculation with a ligninolytic basidiomycete, but not root symbiotic ascomycetes, positively affects growth of highbush blueberry (Ericaceae) grown in a pine litter substrate. Plant Soil 355, 341–352 (2012). https://doi.org/10.1007/s11104-011-1106-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-011-1106-2

Keywords

Search

Navigation